Preferences help
enabled [disable] Abstract
Number of results
2003 | 50 | 2 | 297-318
Article title

Thermodynamics of specific protein-RNA interactions.

Title variants
Languages of publication
Description of the recognition specificity between proteins and nucleic acids at the level of molecular interactions is one of the most challenging tasks in biophysics. It is key to understanding the course and control of gene expression and to the application of the thus acquired knowledge in chemotherapy. This review presents experimental results of thermodynamic studies and a discussion of the role of thermodynamics in formation and stability of functional protein-RNA complexes, with a special attention to the interactions involving mRNA 5' cap and cap-binding proteins in the initiation of protein biosynthesis in the eukaryotic cell. A theoretical framework for analysis of the thermodynamic parameters of protein-nucleic acid association is also briefly surveyed. Overshadowed by more spectacular achievements in structural studies, the thermodynamic investigations are of equal importance for full comprehension of biopolymers' activity in a quantitative way. In this regard, thermodynamics gives a direct insight into the energetic and entropic characteristics of complex macromolecular systems in their natural environment, aqueous solution, and thus complements the structural view derived from X-ray crystallography and multidimensional NMR. Further development of the thermodynamic approach toward interpretation of recognition and binding specificity in terms of molecular biophysics requires more profound contribution from statistical mechanics.
Physical description
  • Department of Biophysics, Institute of Experimental Physics, Warsaw University, Warszawa, Poland
  • Amzel LM. (1997) Loss of translational entropy in binding, folding, and catalysis. Proteins.; 28: 144-9.
  • Arnez JG, Cavarelli J. (1997) Structures of RNA-binding proteins. Q Rev Biophys.; 30: 195-240.
  • Baidya N, Uhlenbeck OC. (1995) The role of 2'-hydroxyl groups in an RNA-protein interaction. Biochemistry.; 34: 12363-8.
  • Baker BM, Murphy KP. (1996) Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys J.; 71: 2049-55.
  • Baldwin RL. (1986) Temperature dependence of the hydrophobic interaction in protein folding. Proc Natl Acad Sci U S A.; 83: 8069-72.
  • Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science.; 289: 905-20.
  • Batey RT, Sagar MB, Doudna JA. (2001) Structural and energetic analysis of RNA recognition by a universally conserved protein from the signal recognition particle. J Mol Biol.; 307: 229-46.
  • Baumann C, Otridge J, Gollnick P. (1996) Kinetic and thermodynamic analysis of the interaction between TRAP (trp RNA-binding attenuation protein) of Bacillus subtilis and trp leader RNA. J Biol Chem.; 271: 12269-74.
  • Beaudette NV, Langerman N. (1980) The thermodynamics of nucleotide binding to proteins. CRC Crit Rev Biochem.; 9: 145-70.
  • Blachut-Okrasinska E, Bojarska E, Niedzwiecka A, Chlebicka L, Darzynkiewicz E, Stolarski R, Stepinski J, Antosiewicz JM. (2000) Stopped-flow and Brownian dynamics studies of electrostatic effects in the kinetics of binding of 7-methyl-GpppG to the protein eIF4E. Eur Biophys J.; 29: 487-98.
  • Boresch S, Archontis G, Karplus M. (1994) Free energy simulations: the meaning of the individual contributions from a component analysis. Proteins.; 20: 25-33.
  • Brauns EB, Madaras ML, Coleman RS, Murphy CJ, Berg MA. (1999) Measurement of local DNA reorganization on the picosecond and nanosecond time scales. J Am Chem Soc.; 121: 11644-9.
  • Brown MJ, Mensah LM, Doyle ML, Broom NJ, Osbourne N, Forrest AK, Richardson CM, O'Hanlon PJ, Pope AJ. (2000) Rational design of femtomolar inhibitors of isoleucyl tRNA synthetase from a binding model for pseudomonic acid-A. Biochemistry.; 39: 6003-11.
  • Bruzzese FJ, Connelly PR. (1997) Allosteric properties of inosine monophosphate dehydrogenase revealed through the thermodynamics of binding of inosine 5'-monophosphate and mycophenolic acid. Temperature dependent heat capacity of binding as a signature of ligand-coupled conformational equilibria. Biochemistry.; 36: 10428-38.
  • Calero G, Wilson KF, Ly T, Rios-Steiner JL, Clardy JC, Cerione RA. (2002) Structural basis of m7GpppG binding to the nuclear cap-binding protein complex. Nat Struct Biol.; 9: 912-7.
  • Cameron KS, Fielding L. (2001) NMR diffusion spectroscopy as a measure of host-guest complex association constants and as a probe of complex size. J Org Chem.; 66: 6891-5.
  • Caprara MG, Myers CA, Lambowitz AM. (2001) Interaction of the Neurospora crassa mitochondrial tyrosyl-tRNA synthetase (CYT-18 protein) with the group I intron P4-P6 domain. Thermodynamic analysis and the role of metal ions. J Mol Biol.; 308: 165-90.
  • Carberry SE, Rhoads RE, Goss DJ. (1989) A spectroscopic study of the binding of m7GTP and m7GpppG to human protein synthesis initiation factor 4E. Biochemistry.; 28: 8078-83.
  • Carey J, Uhlenbeck OC. (1983) Kinetic and thermodynamic characterization of the R17 coat protein-ribonucleic acid interaction. Biochemistry.; 22: 2610-5.
  • Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature.; 407: 340-8.
  • Chaires JB. (1997a) Energetics of drug-DNA interactions. Biopolymers.; 44: 201-15.
  • Chaires JB. (1997b) Possible origin of differences between van't Hoff and calorimetric enthalpy estimates. Biophys J.; 64: 15-23.
  • Chaires JB, Satyanarayana S, Suh D, Fokt I, Przewloka T, Priebe W. (1996) Parsing the free energy of anthracycline antibiotic binding to DNA. Biochemistry.; 35: 2047-53.
  • Chaires JB, Sturtevant JM. (1986) Thermodynamics of the B to Z transition in poly(m5dG-dC). Proc Natl Acad Sci U S A.; 83: 5479-83.
  • Chance MR, Bresnick AR, Burley SK, Jiang JS, Lima CD, Sali A, Almo SC, Bonanno JB, Buglino JA, Boulton S, Chen H, Eswar N, He G, Huang R, Ilyin V, McMahan L, Pieper U, Ray S, Vidal M, Wang LK. (2002) Structural genomics: a pipeline for providing structures for the biologist. Protein Sci.; 11: 723-38.
  • Cho Y, Gorina S, Jeffrey PD, Pavletich NP. (1994) Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science.; 265: 346-55.
  • Cooper A, Johnson CM, Lakey JH, Nollmann M. (2001) Heat does not come in different colours: entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions. Biophys Chem.; 93: 215-30.
  • Day YS, Baird CL, Rich RL, Myszka DG. (2002) Direct comparison of binding equilibrium, thermodynamic, and rate constants determined by surface- and solution-based biophysical methods. Protein Sci.; 11: 1017-25.
  • den Blaauwen T, van der Wolk JP, van der Does C, van Wely KH, Driessen AJ. (1999) Thermodynamics of nucleotide binding to NBS-I of the Bacillus subtilis preprotein translocase subunit SecA. FEBS Lett.; 458: 145-50.
  • Derrick TS, McCord EF, Larive CK. (2002) Analysis of protein/ligand interactions with NMR diffusion measurements: the importance of eliminating the protein background. J Magn Reson.; 155: 217-25.
  • Dever TE. (2002) Gene-specific regulation by general translation factors. Cell.; 108: 545-56.
  • Draper DE. (1995) Protein-RNA recognition. Annu Rev Biochem.; 64: 593-620.
  • Draper DE. (1999) Themes in RNA-protein recognition. J Mol Biol.; 293: 255-70.
  • Eftink MR. (1997) Fluorescence methods for studying equilibrium macromolecule-ligand interactions. Methods Enzymol.; 278: 221-57.
  • Eftink MR, Anusiem AC, Biltonen RL. (1983) Enthalpy-entropy compensation and heat capacity changes for protein-ligand interactions: general thermodynamic models and data for the binding of nucleotides to ribonuclease A. Biochemistry.; 22: 3884-96.
  • Elliott M, Gottlieb P, Gollnick P. (2001) Using nucleotide analogs to probe protein-RNA interactions. Methods.; 23: 255-63.
  • Fidalgo S, Mandal SS, Reha-Krantz LJ. (2002) Using 2-aminopurine fluorescence to measure incorporation of incorrect nucleotides by wild type and mutant bacteriophage T4 DNA polymerases. J Biol Chem.; 277: 40640-9.
  • Fielding L. (2000) Determination of association constants (Ka) from solution NMR data. Tetrahedron.; 56: 6151-70.
  • Fischer WF, Zeng L, Pang Y, Hu W, Majumdar A, Zuiderweg ERP. (1997) Experimental characterization of models for backbone picosecond dynamics in proteins. Qualification of NMR auto- and cross-correlation relaxation mechanisms involving different nuclei of the peptide plane. J Am Chem Soc.; 119: 12629-42.
  • Fisher HF, Singh N. (1995) Calorimetric methods for interpreting protein-ligand interactions. Methods Enzymol.; 259: 194-221.
  • Fivash M, Towler EM, Fisher RJ. (1998) BIAcore for macromolecular interaction. Curr Opin Biotechnol.; 9: 97-101.
  • Forstner M, Berger C, Wallimann T. (1999) Nucleotide binding to creatine kinase: an isothermal titration microcalorimetry study. FEBS Lett.; 461: 111-4.
  • Freire E. (1998) Statistical thermodynamic linkage between conformational and binding equilibria. Adv Protein Chem.; 51: 255-79.
  • Gallagher K, Sharp K. (1998) Electrostatic contributions to heat capacity changes of DNA-ligand binding. Biophys J.; 75: 769-76.
  • Garcia-Fuentes L, Camara-Artigas A, Lopez-Mayorga O, Baron C. (1996a) A calorimetric study of the binding of AMP to liver glycogen phosphorylase b. Biochim Biophys Acta.; 1294: 83-8.
  • Garcia-Fuentes L, Camara-Artigas A, Lopez-Mayorga O, Baron C. (1996b) Thermodynamic characterization of 5'-AMP binding to bovine liver glycogen phosphorylase a. J Biol Chem.; 271: 27569-74.
  • Garcia-Fuentes L, Reche P, Lopez-Mayorga O, Santi DV, Gonzalez-Pacanowska D, Baron C. (1995) Thermodynamic analysis of the binding of 5-fluoro-2'-deoxyuridine 5'- monophosphate to thymidylate synthase over a range of temperatures. Eur J Biochem.; 232: 641-5.
  • Garvie CW, Wolberger C. (2001) Recognition of specific DNA sequences. Mol Cell.; 8: 937-46.
  • Gessi S, Varani K, Merighi S, Morelli A, Ferrari D, Leung E, Baraldi PG, Spalluto G, Borea PA. (2001) Pharmacological and biochemical characterization of A3 adenosine receptors in Jurkat T cells. Br J Pharmacol.; 134: 116-26.
  • Gilson MK, Given JA, Bush BL, McCammon JA. (1997) The statistical-thermodynamic basis for computation of binding affinities: a critical review. Biophys J.; 72: 1047-69.
  • Gingras AC, Raught B, Sonenberg N. (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem.; 68: 913-63.
  • Gohlke H, Klebe G. (2002) Approaches to the description and prediction of the binding affinity of small-molecule ligands to macromolecular receptors. Angew Chem Int Ed Engl.; 41: 2644-76.
  • Gomez J, Hilser VJ, Xie D, Freire E. (1995) The heat capacity of proteins. Proteins.; 22: 404-12.
  • Gosse C, Croquette V. (2002) Magnetic tweezers: micromanipulation and force measurement at the molecular level. Biophys J.; 82: 3314-29.
  • Ha JH, Spolar RS, Record MT Jr. (1989) Role of the hydrophobic effect in stability of site-specific protein-DNA complexes. J Mol Biol.; 209: 801-16.
  • Hall KB, Stump WT. (1992) Interaction of N-terminal domain of U1A protein with an RNA stem/loop. Nucleic Acids Res.; 20: 4283-90.
  • Haun MF, Wirth M, Ruterjans H. (1995) Calorimetric investigation of thermal stability and ligand-binding characteristics of disulfide-bond-cleaved ribonuclease T1. Eur J Biochem.; 227: 516-23.
  • Hermann T, Patel DJ. (2000) Adaptive recognition by nucleic acid aptamers. Science.; 287: 820-5.
  • Hermans J, Wang L. (1997) Inclusion of loss of translational and rotational freedom in theoretical estimates of free energies of binding. Application to a complex of benzene and mutant T4 lysozyme. J Amer Chem Soc.; 119: 2707-14.
  • Hileman RE, Jennings RN, Linhardt RJ. (1998) Thermodynamic analysis of the heparin interaction with a basic cyclic peptide using isothermal titration calorimetry. Biochemistry.; 37: 15231-7.
  • Hodel AE, Gershon PD, Quiocho FA. (1998) Structural basis for sequence-nonspecific recognition of 5'-capped mRNA by a cap-modifying enzyme. Mol Cell.; 1: 443-7.
  • Hodel AE, Gershon PD, Shi X, Wang SM, Quiocho FA. (1997) Specific protein recognition of an mRNA cap through its alkylated base. Nat Struct Biol.; 4: 350-4.
  • Horn JR, Russell D, Lewis EA, Murphy KP. (2001) Van't Hoff and calorimetric enthalpies from isothermal titration calorimetry: are there significant discrepancies? Biochemistry.; 40: 1774-8.
  • Horn JR, Brandts JF, Murphy KP. (2002) Van't Hoff and calorimetric enthalpies II: effects of linked equilibria. Biochemistry.; 41: 7501-7.
  • Hu CQ, Sturtevant JM. (1992) Thermodynamics of binding of mononucleotides to ribonuclease T1. J Phys Chem.; 96: 4052-6.
  • Israelachvili J, Wennerstrom H. (1996) Role of hydration and water structure in biological and colloidal interactions. Nature.; 379: 219-25.
  • Jayaram B, McConnell KJ, Dixit SB, Beveridge DL. (1999) Free energy analysis of protein-DNA binding: the EcoRI endonuclease-DNA complex. J Comput Phys.; 151: 333-7.
  • Jin L, Yang J, Carey J. (1993) Thermodynamics of ligand binding to trp repressor. Biochemistry.; 32: 7302-9.
  • Johansson HE, Dertinger D, LeCuyer KA, Behlen LS, Greef CH, Uhlenbeck OC. (1998) A thermodynamic analysis of the sequence-specific binding of RNA by bacteriophage MS2 coat protein. Proc Natl Acad Sci U S A.; 95: 9244-9.
  • Johnson KA. (1992) Transient-state kinetic analysis of enzyme reaction pathways. Enzymes.; 20: 1-61.
  • Jones S, van Heyningen P, Berman HM, Thornton JM. (1999) Protein-DNA interactions: A structural analysis. J Mol Biol.; 287: 877-96.
  • Karplus M, McCammon JA. (1981) The internal dynamics of globular proteins. CRC Crit Rev Biochem.; 9: 293-349.
  • Karplus M, Petsko GA. (1990) Molecular dynamics simulations in biology. Nature.; 347: 631-9.
  • Karplus M, Ichiye T, Pettitt BM. (1987) Configurational entropy of native proteins. Biophys J.; 52: 1083-5.
  • Kiraga-Motoszko K, Stepinski J, Niedzwiecka A, Jemielity J, Wszelaka-Rychlik M, Stolarski R, Zielenkiewicz W, Darzynkiewicz E. (2003) Interaction between yeast eukaryotic initiation factor eIF4E and mRNA 5' cap analogues differ from that for murine eIF4E. Nucleosides Nucleotides Nucl Acids.; in press.
  • Koloteva N, Muller PP, McCarthy JE. (1997) The position dependence of translational regulation via RNA-RNA and RNA-protein interactions in the 5'-untranslated region of eukaryotic mRNA is a function of the thermodynamic competence of 40 S ribosomes in translational initiation. J Biol Chem.; 272: 16531-9.
  • Kozlov AG, Lohman TM. (1999) Adenine base unstacking dominates the observed enthalpy and heat capacity changes for the Escherichia coli SSB tetramer binding to single-stranded oligoadenylates. Biochemistry.; 38: 7388-97.
  • Kranz JK, Hall KB. (1998) RNA binding mediates the local cooperativity between the beta-sheet and the C-terminal tail of the human U1A RBD1 protein. J Mol Biol.; 275: 465-81.
  • Kranz JK, Hall KB. (1999) RNA recognition by the human U1A protein is mediated by a network of local cooperative interactions that create the optimal binding surface. J Mol Biol.; 285: 215-31.
  • Krupakar J, Swaminathan CP, Das PK, Surolia A, Podder SK. (1999) Calorimetric studies on the stability of the ribosome-inactivating protein abrin II: effects of pH and ligand binding. Biochem J.; 338: 273-9.
  • Kuntz ID, Chen K, Sharp KA, Kollman PA. (1999) The maximal affinity of ligands. Proc Natl Acad Sci U S A.; 96: 9997-10002.
  • Ladbury JE, Wright JG, Sturtevant JM, Sigler PB. (1994) A thermodynamic study of the trp repressor-operator interaction. J Mol Biol.; 238: 669-81.
  • Lanzilotta WN, Parker VD, Seefeldt LC. (1999) Thermodynamics of nucleotide interactions with the Azotobacter vinelandii nitrogenase iron protein. Biochim Biophys Acta.; 1429: 411-21.
  • LaRiviere FJ, Wolfson AD, Uhlenbeck OC. (2001) Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science.; 294: 165-8.
  • Laws WR, Contino PB. (1992) Fluorescence quenching studies: analysis of nonlinear Stern-Volmer data. Methods Enzymol.; 210: 448-63.
  • Lee KH, Xie D, Freire E, Amzel LM. (1994) Estimation of changes in side chain configurational entropy in binding and folding: general methods and application to helix formation. Proteins.; 20: 68-84.
  • Lesyng B, McCammon JA. (1993) Molecular modeling methods. Basic techniques and challenging problems. Pharmacol Ther.; 60: 149-67.
  • Liu Y, Sturtevant JM. (1995) Significant discrepancies between van't Hoff and calorimetric enthalpies. II. Protein Sci.; 4: 2559-61.
  • Liu Y, Sturtevant JM. (1997) Significant discrepancies between van't Hoff and calorimetric enthalpies. III. Biophys Chem.; 64: 121-6.
  • Livingstone JR, Spolar RS, Record MT Jr. (1991) Contribution to the thermodynamics of protein folding from the reduction in water-accessible nonpolar surface area. Biochemistry.; 30: 4237-44.
  • Lohman TM, Overman LB, Ferrari ME, Kozlov AG. (1996) A highly salt-dependent enthalpy change for Escherichia coli SSB protein-nucleic acid binding due to ion-protein interactions. Biochemistry.; 35: 5272-9.
  • Londei P. (1998) A hypothesis on the mechanism of translational initiation. Biochim Biophys Acta.; 1396: 169-78.
  • Lorsch JR, Herschlag D. (1998) The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry.; 37: 2180-93.
  • Lostao A, El Harrous M, Daoudi F, Romero A, Parody-Morreale A, Sancho J. (2000) Dissecting the energetics of the apoflavodoxin-FMN complex. J Biol Chem.; 275: 9518-26.
  • Luo H, Sharp K. (2002) On the calculation of absolute macromolecular binding free energies. Proc Natl Acad Sci U S A.; 99: 10399-404.
  • Luther MA, Cai GZ, Lee JC. (1986) Thermodynamics of dimer and tetramer formations in rabbit muscle phosphofructokinase. Biochemistry.; 25: 7931-7.
  • Madan B, Sharp K. (2003) Changes in water structure induced by a hydrophobic solute probed by simulation of the water hydrogen bond angle and radial distribution functions. Biophys Chem.; 78: 33-41.
  • Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. (1997) Cocrystal structure of the messenger RNA 5' cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell.; 89: 951-61.
  • Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. (1999) Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell.; 3: 707-16.
  • Mark AE, van Gunsteren WF. (1994) Decomposition of the free energy of a system in terms of specific interactions. Implications for theoretical and experimental studies. J Mol Biol.; 240: 167-76.
  • Matsuo H, Li H, McGuire AM, Fletcher CM, Gingras AC, Sonenberg N, Wagner G. (1997) Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat Struct Biol.; 4: 717-24.
  • Matulis D, Rouzina I, Bloomfield VA. (2000) Thermodynamics of DNA binding and condensation: isothermal titration calorimetry and electrostatic mechanism. J Mol Biol.; 296: 1053-63.
  • Mazza C, Segref A, Mattaj IW, Cusack S. (2002) Large-scale induced fit recognition of an m(7)GpppG cap analogue by the human nuclear cap-binding complex. EMBO J.; 21: 5548-57.
  • McCarthy JE. (1998) Posttranscriptional control of gene expression in yeast. Microbiol Mol Biol Rev.; 62: 1492-553.
  • Meyer EA, Castellano RK, Diederich F. (2003) Interactions with aromatic rings in chemical and biochemical recognition. Angew Chem Int Ed Engl.; 42: 1210-50.
  • Millar DP. (2000) Time-resolved fluorescence methods for analysis of DNA-protein interactions. Methods Enzymol.; 323: 442-59.
  • Mougel M, Ehresmann B, Ehresmann C. (1986) Binding of Escherichia coli ribosomal protein S8 to 16S rRNA: kinetic and thermodynamic characterization. Biochemistry.; 25: 2756-65.
  • Murphy KP. (1999) Predicting binding energetics from structure: looking beyond DeltaG degrees. Med Res Rev.; 19: 333-9.
  • Murphy KP, Bhakuni V, Xie D, Freire E. (1992) Molecular basis of co-operativity in protein folding. III. Structural identification of cooperative folding units and folding intermediates. J Mol Biol.; 227: 293-306.
  • Murphy KP, Freire E. (1992) Thermodynamics of structural stability and cooperative folding behavior in proteins. Adv Protein Chem.; 43: 313-61.
  • Murphy KP, Privalov PL, Gill SJ. (1990) Common features of protein unfolding and dissolution of hydrophobic compounds. Science.; 247: 559-61.
  • Naghibi H, Tamura A, Sturtevant JM. (1995) Significant discrepancies between van't Hoff and calorimetric enthalpies. Proc Natl Acad Sci U S A.; 92: 5597-9.
  • Niedzwiecka-Kornas A, Przedmojski R, Balaspiri L, Wieczorek Z, Stepinski J, Jankowska M, Lonnberg H, Darzynkiewicz E, Stolarski R. (1999) Studies on association of mRNA cap-analogues with a synthetic dodecapeptide DGIEPMWEDEKN. Nucleosides Nucleotides.; 18: 1105-6.
  • Niedzwiecka A, Marcotrigiano J, Stepinski J, Jankowska-Anyszka M, Wyslouch-Cieszynska A, Dadlez M, Gingras AC, Mak P, Darzynkiewicz E, Sonenberg N, Burley SK, Stolarski R. (2002a) Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 5' cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins. J Mol Biol.; 319: 615-35.
  • Niedzwiecka A, Stepinski J, Darzynkiewicz E, Sonenberg N, Stolarski R. (2002b) Positive heat capacity change upon specific binding of translation initiation factor eIF4E to mRNA 5' cap. Biochemistry.; 41: 12140-8.
  • Niedzwiecka A, Stepinski J, Balaspiri J, Darzynkiewicz E, Stolarski R. (2003) Thermodynamics of 7-methylguanosine cation stacking with tryptophan upon mRNA 5' cap binding to translation factor eIF4E. Nucleosides Nucleotides Nucl Acids.; in press.
  • Nierhaus KH, Schilling-Bartetzko S, Twardowski T. (1992) The two main states of the elongating ribosome and the role of the alpha-sarcin stem-loop structure of 23S RNA. Biochimie.; 74: 403-10.
  • Nomanbhoy T, Morales AJ, Abraham A.T, Vortler CS, Giege R, Schimmel P. (2001) Simultaneous binding of two proteins to opposite sides of a single transfer RNA. Nat Struct Biol.; 8: 344-8.
  • Oberfelder RW, Lee JC. (1985) Measurement of ligand-protein interaction by electrophoretic and spectroscopic techniques. Methods Enzymol.; 117: 381-99.
  • Oda M, Furukawa K, Ogata K, Sarai A, Nakamura H. (1998) Thermodynamics of specific and non-specific DNA binding by the c-Myb DNA-binding domain. J Mol Biol.; 276: 571-90.
  • Oda M, Nakamura H. (2000) Thermodynamic and kinetic analyses for understanding sequence-specific DNA recognition. Genes Cells.; 5: 319-26.
  • Odaka M, Kaibara C, Amano T, Matsui T, Muneyuki E, Ogasahara K, Yutani K, Yoshida M. (1994) Tyr-341 of the beta subunit is a major Km-determining residue of TF1- ATPase: parallel effect of its mutations on Kd(ATP) of the beta subunit and on Km(ATP) of the alpha 3 beta 3 gamma complex. J Biochem.; 115: 789-96.
  • Parkhurst KM, Hileman RE, Saha D, Gupta NK, Parkhurst LJ. (1994) Thermodynamic characterization of the cooperativity of 40S complex formation during the initiation of eukaryotic protein synthesis. Biochemistry.; 33: 15168-77.
  • Parsegian VA, Rand RP, Rau DC. (1995) Macromolecules and water: probing with osmotic stress. Methods Enzymol.; 259: 43-94.
  • Patikoglou G, Burley SK. (1997) Eukaryotic transcription factor-DNA complexes. Annu Rev Biophys Biomol Struct.; 26: 289-325.
  • Pervushin K, Riek R, Wider G, Wuthrich K. (1997) Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci U S A.; 94: 12366-71.
  • Pitici F, Beveridge DL, Baranger AM. (2002) Molecular dynamics simulation studies of induced fit and conformational capture in U1A-RNA binding: do molecular substates code for specificity? Biopolymers.; 65: 424-35.
  • Pleiss JA, Uhlenbeck OC. (2001) Identification of thermodynamically relevant interactions between EF-Tu and backbone elements of tRNA. J Mol Biol.; 308: 895-905.
  • Plum GE, Breslauer KJ. (1995) Calorimetry of proteins and nucleic acids. Curr Opin Struct Biol.; 5: 682-90.
  • Polach KJ, Uhlenbeck OC. (2002) Cooperative binding of ATP and RNA substrates to the DEAD/H protein DbpA. Biochemistry.; 41: 3693-702.
  • Praefcke GJ, Geyer M, Schwemmle M, Robert KH, Herrmann C. (1999) Nucleotide-binding characteristics of human guanylate-binding protein 1 (hGBP1) and identification of the third GTP-binding motif. J Mol Biol.; 292: 321-32.
  • Raught B, Gingras AC. (1999) eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol.; 31: 43-57.
  • Record MT Jr, Ha JH, Fisher MA. (1991) Analysis of equilibrium and kinetic measurements to determine thermodynamic origins of stability and specificity and mechanism of formation of site-specific complexes between proteins and helical DNA. Methods Enzymol.; 208: 291-343.
  • Reyes CM. Kollman PA. (2000) Structure and thermodynamics of RNA-protein binding: using molecular dynamics and free energy analyses to calculate the free energies of binding and conformational change. J Mol Biol.; 297: 1145-58.
  • Ribas P, Auld DS, Kim S, Schimmel P. (1996) A mechanism for reducing entropic cost of induced fit in protein-RNA recognition. Biochemistry.; 35: 8095-102.
  • Riek R, Fiaux J, Bertelsen EB, Horwich AL, Wuthrich K. (2002) Solution NMR techniques for large molecular and supramolecular structures. J Am Chem Soc.; 124: 12144-53.
  • Riek R, Wider G, Pervushin K, Wuthrich K. (1999). Polarization transfer by cross-correlated relaxation in solution NMR with very large molecules. Proc Natl Acad Sci U S A.; 96: 4918-23.
  • Robinson BH, Drobny GP. (1995) Site-specific dynamics in DNA: theory and experiment. Methods Enzymol.; 261: 451-509.
  • Rosgen J, Hallerbach B, Hinz HJ. (1998) The 'Janus' nature of proteins: systems at the verge of the microscopic and macroscopic world. Biophys Chem.; 74: 153-61.
  • Rosgen J, Hinz HJ. (2002) The heat capacity paradox of ligand binding proteins: reconciling the microscopic and macroscopic world. Biophys Chem.; 96: 109-16.
  • Rouzina I, Bloomfield VA. (1999) Heat capacity effects on the melting of DNA. 1. General aspects. Biophys J.; 77: 3242-51.
  • Sachs AB, Sarnow P, Hentze MW. (1997) Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell.; 89: 831-8.
  • Sarai A, Gromiha MM, An J, Prabakaran P, Selvaraj S, Kono H, Oobatake M, Uedaira H. (2001) Thermodynamic databases for proteins and protein-nucleic acid interactions. Biopolymers.; 61: 121-6.
  • Schafer H, Smith LJ, Mark AE, van Gunsteren WF. (2002) Entropy calculations on the molten globule state of a protein: side-chain entropies of alpha-lactalbumin. Proteins.; 46: 215-24.
  • Scheibel T, Siegmund HI, Jaenicke R, Ganz P, Lilie H, Buchner J. (1999) The charged region of Hsp90 modulates the function of the N-terminal domain. Proc Natl Acad Sci USA.; 96: 1297-1302.
  • Schluenzen F, Tocilj A, Zarivach R, Harms J, Gluehmann M, Janell D, Bashan A, Bartels H, Agmon I, Franceschi F, Yonath A. (2000) Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell.; 102: 615-23.
  • Schneider H-J. (1991) Mechanisms of molecular recognition: investigations of organic host-guest complexes. Angew Chem Int Ed Engl.; 30: 1417-36.
  • Schwabe JW. (1997) The role of water in protein-DNA interactions. Curr Opin Struct Biol.; 7: 126-34.
  • Sharp K. (2001) Entropy-enthalpy compensation: fact or artifact? Protein Sci.; 10: 661-7.
  • Shatkin AJ, Darzynkiewicz E, Furuichi Y, Kroath H, Morgan MA, Tahara SM, Yamakawa M. (1982) 5'-Terminal caps, cap-binding proteins and eukaryotic mRNA function. Biochem Soc Symp.; 47: 129-43.
  • Shen X, Tomoo K, Uchiyama S, Kobayashi Y, Ishida T. (2001) Structural and thermodynamic behavior of eukaryotic initiation factor 4E in supramolecular formation with 4E-binding protein 1 and mRNA cap analogue, studied by spectroscopic methods. Chem Pharm Bull.; 49: 1299-1303.
  • Silverstein KAT, Haymet ADJ, Dill KA. (1998) A simple model of water and the hydrophobic effect. J Am Chem Soc.; 120: 3136-75.
  • Simmons RM, Finer JT, Chu S, Spudich JA. (1996) Quantitative measurements of force and displacement using an optical trap. Biophys J.; 70: 1813-22.
  • Singh N, Fisher HF. (1994) Protein-ligand interactions as a driving force for a high-enthalpy two-state transition in glutamate dehydrogenase: the opposing roles of phosphate and acetate ions. Arch Biochem Biophys.; 312: 38-44.
  • Spolar RS, Livingstone JR, Record MT Jr. (1992) Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water. Biochemistry.; 31: 3947-55.
  • Spolar RS, Record MT Jr. (1994) Coupling of local folding to site-specific binding of proteins to DNA. Science.; 263: 777-84.
  • Stark H, Dube P, Luhrmann R, Kastner B. (2001) Arrangement of RNA and proteins in the spliceosomal U1 small nuclear ribonucleoprotein particle. Nature.; 409: 539-42.
  • Stolz M, Stoffler D, Aebi U, Goldsbury C. (2000) Monitoring biomolecular interactions by time-lapse atomic force microscopy. J Struct Biol.; 131: 171-80.
  • Sturtevant JM. (1977) Heat capacity and entropy changes in processes involving proteins. Proc Natl Acad Sci U S A.; 74: 2236-40.
  • Szabo A, Stolz L, Granzow R. (1995) Surface plasmon resonance and its use in biomolecular interaction analysis (BIA). Curr Opin Struct Biol.; 5: 699-705.
  • Talbot SJ, Altman S. (1994a) Gel retardation analysis of the interaction between C5 protein and M1 RNA in the formation of the ribonuclease P holoenzyme from Escherichia coli. Biochemistry.; 33: 1399-1405.
  • Talbot SJ, Altman S. (1994b) Kinetic and thermodynamic analysis of RNA-protein interactions in the RNase P holoenzyme from Escherichia coli. Biochemistry.; 33: 1406-11.
  • Tellez-Sanz R, Bernier-Villamor V, Garcia-Fuentes L, Gonzalez-Pacanowska D, Baron C. (1997) Thermodynamic characterization of the binding of dCMP to the Asn229Asp mutant of thymidylate synthase. FEBS Lett.; 409: 385-90.
  • Terada TP, Kuwajima K. (1999) Thermodynamics of nucleotide binding to the chaperonin GroEL studied by isothermal titration calorimetry: evidence for noncooperative nucleotide binding. Biochim Biophys Acta.; 1431: 269-81.
  • Tomoo K, Shen X, Okabe K, Nozoe Y, Fukuhara S, Morino S, Ishida T, Taniguchi T, Hasegawa H, Terashima A, Sasaki M, Katsuya Y, Kitamura K, Miyoshi H, Ishikawa M, Miura K. (2002) Crystal structures of 7-methylguanosine 5'-triphosphate (m(7)GTP)- and P(1)-7-methylguanosine-P(3)- adenosine-5',5'-triphosphate (m(7)GpppA)- bound human full-length eukaryotic initiation factor 4E: biological importance of the C-terminal flexible region. Biochem J.; 362: 539-44.
  • Tsai CJ, Maizel JV Jr, Nussinov R. (2002) The hydrophobic effect: a new insight from cold denaturation and a two-state water structure. Crit Rev Biochem Mol Biol.; 37: 55-69.
  • van Gunsteren WF, Berendsen HJC. (1990) Computer simulation of molecular dynamics: methodology, application, and perspectives in chemistry. Angew Chem Int Ed Engl.; 29: 992-1023.
  • Varani G, Nagai K. (1998) RNA recognition by RNP proteins during RNA processing. Annu Rev Biophys Biomol Struct.; 27: 407-45.
  • von der Haar T, Ball PD, McCarthy JE. (2000) Stabilization of eukaryotic initiation factor 4E binding to the mRNA 5'- cap by domains of eIF4G. J Biol Chem.; 275: 30551-5.
  • Wallis R, Moore GR, James R, Kleanthous C. (1995) Protein-protein interactions in colicin E9 DNase-immunity protein complexes. 1. Diffusion-controlled association and femtomolar binding for the cognate complex. Biochemistry.; 34: 13743-50.
  • Wang ZX. (1995) An exact mathematical expression for describing competitive binding of two different ligands to a protein molecule. FEBS Lett.; 360: 111-4.
  • Weeks KM. (1997) Protein-facilitated RNA folding. Curr Opin Struct Biol.; 7: 336-42.
  • Weiss S. (1999) Fluorescence spectroscopy of single biomolecules. Science.; 283: 1676-83.
  • Werner M. (1991) Kinetic and thermodynamic characterization of the interaction between Q beta-replicase and template RNA molecules. Biochemistry.; 30: 5832-8.
  • Williams DJ, Hall KB. (1996) RNA hairpins with non-nucleotide spacers bind efficiently to the human U1A protein. J Mol Biol.; 257: 265-75.
  • Wilson GM, Sutphen K, Bolikal S, Chuang KY, Brewer G. (2001) Thermodynamics and kinetics of Hsp70 association with A+ U-rich mRNA-destabilizing sequences. J Biol Chem.; 276: 44450-6.
  • Wimberly BT, Brodersen DE, Clemons WM Jr, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V. (2000) Structure of the 30S ribosomal subunit. Nature.; 407: 327-39.
  • Wiseman T, Williston S, Brandts JF, Lin LN. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem.; 179: 131-7.
  • Wu P, Sugimoto N. (2000) Transition characteristics and thermodynamic analysis of DNA duplex formation: a quantitative consideration for the extent of duplex association. Nucleic Acids Res.; 28: 4762-8.
  • Xu Y, Johnson CR, Beckett D. (1996) Thermodynamic analysis of small ligand binding to the Escherichia coli repressor of biotin biosynthesis. Biochemistry.; 35: 5509-17.
  • Yee A, Chang X, Pineda-Lucena A, Wu B, Semesi A, Le B, Ramelot T, Lee GM, Bhattacharyya S, Gutierrez P, Denisov A, Lee CH, Cort JR, Kozlov G, Liao J, Finak G, Chen L, Wishart D, Lee W, McIntosh LP, Gehring K, Kennedy MA, Edwards AM, Arrowsmith CH. (2002) An NMR approach to structural proteomics. Proc Natl Acad Sci US A.; 99: 1825-30.
  • Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF. (2001) Crystal structure of the ribosome at 5.5 Å resolution. Science.; 292: 883-96.
  • Zheng X, Bevilacqua PC. (2000) Straightening of bulged RNA by the double-stranded RNA-binding domain from the protein kinase PKR. Proc Natl Acad Sci U S A.; 97: 14162-7.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.