2agw › Citations

Atomic description of an enzyme reaction dominated by proton tunneling.

Masgrau L, Roujeinikova A, Johannissen LO, Hothi P, Basran J, Ranaghan KE, Mulholland AJ, Sutcliffe MJ, Scrutton NS, Leys D
Science 312 237-41 (2006)
Related entries: 2agl, 2agx, 2agy, 2agz, 2ah0, 2ah1

Cited: 122 times
EuropePMC logo PMID: 16614214

Abstract

We present an atomic-level description of the reaction chemistry of an enzyme-catalyzed reaction dominated by proton tunneling. By solving structures of reaction intermediates at near-atomic resolution, we have identified the reaction pathway for tryptamine oxidation by aromatic amine dehydrogenase. Combining experiment and computer simulation, we show proton transfer occurs predominantly to oxygen O2 of Asp(128)beta in a reaction dominated by tunneling over approximately 0.6 angstroms. The role of long-range coupled motions in promoting tunneling is controversial. We show that, in this enzyme system, tunneling is promoted by a short-range motion modulating proton-acceptor distance and no long-range coupled motion is required.

Reviews citing this publication (22)

  1. QM/MM methods for biomolecular systems. Senn HM, Thiel W. Angew Chem Int Ed Engl 48 1198-1229 (2009)
  2. At the dawn of the 21st century: Is dynamics the missing link for understanding enzyme catalysis? Kamerlin SC, Warshel A. Proteins 78 1339-1375 (2010)
  3. Multidimensional tunneling, recrossing, and the transmission coefficient for enzymatic reactions. Pu J, Gao J, Truhlar DG. Chem Rev 106 3140-3169 (2006)
  4. Intracellular pH sensors: design principles and functional significance. Srivastava J, Barber DL, Jacobson MP. Physiology (Bethesda) 22 30-39 (2007)
  5. Hydrogen tunneling in enzymes and biomimetic models. Layfield JP, Hammes-Schiffer S. Chem Rev 114 3466-3494 (2014)
  6. Molecular simulations of protein dynamics: new windows on mechanisms in biology. Dodson GG, Lane DP, Verma CS. EMBO Rep 9 144-150 (2008)
  7. Atom Tunneling in Chemistry. Meisner J, Kästner J. Angew Chem Int Ed Engl 55 5400-5413 (2016)
  8. Hydrogen tunnelling in enzyme-catalysed H-transfer reactions: flavoprotein and quinoprotein systems. Sutcliffe MJ, Masgrau L, Roujeinikova A, Johannissen LO, Hothi P, Basran J, Ranaghan KE, Mulholland AJ, Leys D, Scrutton NS. Philos Trans R Soc Lond B Biol Sci 361 1375-1386 (2006)
  9. The origins of quantum biology. McFadden J, Al-Khalili J. Proc Math Phys Eng Sci 474 20180674 (2018)
  10. Femtochemistry in enzyme catalysis: DNA photolyase. Kao YT, Saxena C, Wang L, Sancar A, Zhong D. Cell Biochem Biophys 48 32-44 (2007)
  11. Ultrafast catalytic processes in enzymes. Zhong D. Curr Opin Chem Biol 11 174-181 (2007)
  12. The importance of ensemble averaging in enzyme kinetics. Masgrau L, Truhlar DG. Acc Chem Res 48 431-438 (2015)
  13. Computational enzymology: insight into biological catalysts from modelling. van der Kamp MW, Mulholland AJ. Nat Prod Rep 25 1001-1014 (2008)
  14. The oxygen-binding vs. oxygen-consuming paradigm in biocatalysis: structural biology and biomolecular simulation. Baron R, McCammon JA, Mattevi A. Curr Opin Struct Biol 19 672-679 (2009)
  15. Structural and mechanistic aspects of flavoproteins: probes of hydrogen tunnelling. Hay S, Pudney CR, Scrutton NS. FEBS J 276 3930-3941 (2009)
  16. Relationship of femtosecond-picosecond dynamics to enzyme-catalyzed H-transfer. Cheatum CM, Kohen A. Top Curr Chem 337 1-39 (2013)
  17. Diversity of structures, catalytic mechanisms and processes of cofactor biosynthesis of tryptophylquinone-bearing enzymes. Yukl ET, Davidson VL. Arch Biochem Biophys 654 40-46 (2018)
  18. Multidimensional insights into the repeated electromagnetic field stimulation and biosystems interaction in aging and age-related diseases. Perez FP, Bandeira JP, Perez Chumbiauca CN, Lahiri DK, Morisaki J, Rizkalla M. J Biomed Sci 29 39 (2022)
  19. Protein dynamics and enzyme catalysis: the ghost in the machine? Glowacki DR, Harvey JN, Mulholland AJ. Biochem Soc Trans 40 515-521 (2012)
  20. Does the pressure dependence of kinetic isotope effects report usefully on dynamics in enzyme H-transfer reactions? Hoeven R, Heyes DJ, Hay S, Scrutton NS. FEBS J 282 3243-3255 (2015)
  21. H-transfers in Photosystem II: what can we learn from recent lessons in the enzyme community? Hay S, Scrutton NS. Photosynth Res 98 169-177 (2008)
  22. New classifications for quantum bioinformatics: Q-bioinformatics, QCt-bioinformatics, QCg-bioinformatics, and QCr-bioinformatics. Mokhtari M, Khoshbakht S, Ziyaei K, Akbari ME, Moravveji SS. Brief Bioinform 25 bbae074 (2024)

Articles citing this publication (100)

  1. Good vibrations in enzyme-catalysed reactions. Hay S, Scrutton NS. Nat Chem 4 161-168 (2012)
  2. Taking Ockham's razor to enzyme dynamics and catalysis. Glowacki DR, Harvey JN, Mulholland AJ. Nat Chem 4 169-176 (2012)
  3. Understanding the kinetics of spin-forbidden chemical reactions. Harvey JN. Phys Chem Chem Phys 9 331-343 (2007)
  4. Artificial enzymes based on supramolecular scaffolds. Dong Z, Luo Q, Liu J. Chem Soc Rev 41 7890-7908 (2012)
  5. Multiple pathways guide oxygen diffusion into flavoenzyme active sites. Baron R, Riley C, Chenprakhon P, Thotsaporn K, Winter RT, Alfieri A, Forneris F, van Berkel WJ, Chaiyen P, Fraaije MW, Mattevi A, McCammon JA. Proc Natl Acad Sci U S A 106 10603-10608 (2009)
  6. Unraveling the role of protein dynamics in dihydrofolate reductase catalysis. Luk LY, Javier Ruiz-Pernía J, Dawson WM, Roca M, Loveridge EJ, Glowacki DR, Harvey JN, Mulholland AJ, Tuñón I, Moliner V, Allemann RK. Proc Natl Acad Sci U S A 110 16344-16349 (2013)
  7. High-accuracy computation of reaction barriers in enzymes. Claeyssens F, Harvey JN, Manby FR, Mata RA, Mulholland AJ, Ranaghan KE, Schütz M, Thiel S, Thiel W, Werner HJ. Angew Chem Int Ed Engl 45 6856-6859 (2006)
  8. Dynamics and dissipation in enzyme catalysis. Boekelheide N, Salomón-Ferrer R, Miller TF. Proc Natl Acad Sci U S A 108 16159-16163 (2011)
  9. Update 1 of: Tunneling and dynamics in enzymatic hydride transfer. Nagel ZD, Klinman JP. Chem Rev 110 PR41-67 (2010)
  10. Conformational changes in an ultrafast light-driven enzyme determine catalytic activity. Sytina OA, Heyes DJ, Hunter CN, Alexandre MT, van Stokkum IH, van Grondelle R, Groot ML. Nature 456 1001-1004 (2008)
  11. Promoting motions in enzyme catalysis probed by pressure studies of kinetic isotope effects. Hay S, Sutcliffe MJ, Scrutton NS. Proc Natl Acad Sci U S A 104 507-512 (2007)
  12. Evidence that a 'dynamic knockout' in Escherichia coli dihydrofolate reductase does not affect the chemical step of catalysis. Loveridge EJ, Behiry EM, Guo J, Allemann RK. Nat Chem 4 292-297 (2012)
  13. Effects of macromolecular crowding on protein conformational changes. Dong H, Qin S, Zhou HX. PLoS Comput Biol 6 e1000833 (2010)
  14. Elusive transition state of alcohol dehydrogenase unveiled. Roston D, Kohen A. Proc Natl Acad Sci U S A 107 9572-9577 (2010)
  15. Remote mutations and active site dynamics correlate with catalytic properties of purine nucleoside phosphorylase. Saen-Oon S, Ghanem M, Schramm VL, Schwartz SD. Biophys J 94 4078-4088 (2008)
  16. Fast enzyme dynamics at the active site of formate dehydrogenase. Bandaria JN, Dutta S, Hill SE, Kohen A, Cheatum CM. J Am Chem Soc 130 22-23 (2008)
  17. Temperature dependence of the kinetic isotope effects in thymidylate synthase. A theoretical study. Kanaan N, Ferrer S, Martí S, Garcia-Viloca M, Kohen A, Moliner V. J Am Chem Soc 133 6692-6702 (2011)
  18. Quantum physics meets biology. Arndt M, Juffmann T, Vedral V. HFSP J 3 386-400 (2009)
  19. An efficient method for the calculation of quantum mechanics/molecular mechanics free energies. Woods CJ, Manby FR, Mulholland AJ. J Chem Phys 128 014109 (2008)
  20. The evolution of multiple active site configurations in a designed enzyme. Hong NS, Petrović D, Lee R, Gryn'ova G, Purg M, Saunders J, Bauer P, Carr PD, Lin CY, Mabbitt PD, Zhang W, Altamore T, Easton C, Coote ML, Kamerlin SCL, Jackson CJ. Nat Commun 9 3900 (2018)
  21. Letter Conformational effects in enzyme catalysis: reaction via a high energy conformation in fatty acid amide hydrolase. Lodola A, Mor M, Zurek J, Tarzia G, Piomelli D, Harvey JN, Mulholland AJ. Biophys J 92 L20-2 (2007)
  22. Metal active site elasticity linked to activation of homocysteine in methionine synthases. Koutmos M, Pejchal R, Bomer TM, Matthews RG, Smith JL, Ludwig ML. Proc Natl Acad Sci U S A 105 3286-3291 (2008)
  23. Examination of enzymatic H-tunneling through kinetics and dynamics. Bandaria JN, Cheatum CM, Kohen A. J Am Chem Soc 131 10151-10155 (2009)
  24. Barrier compression and its contribution to both classical and quantum mechanical aspects of enzyme catalysis. Hay S, Johannissen LO, Sutcliffe MJ, Scrutton NS. Biophys J 98 121-128 (2010)
  25. Computational enzymology. Lonsdale R, Ranaghan KE, Mulholland AJ. Chem Commun (Camb) 46 2354-2372 (2010)
  26. Nitrogenase: a general hydrogenator of small molecules. Dance I. Chem Commun (Camb) 49 10893-10907 (2013)
  27. Exploring the conformational and reactive dynamics of biomolecules in solution using an extended version of the glycine reactive force field. Monti S, Corozzi A, Fristrup P, Joshi KL, Shin YK, Oelschlaeger P, van Duin AC, Barone V. Phys Chem Chem Phys 15 15062-15077 (2013)
  28. The role of large-scale motions in catalysis by dihydrofolate reductase. Loveridge EJ, Tey LH, Behiry EM, Dawson WM, Evans RM, Whittaker SB, Günther UL, Williams C, Crump MP, Allemann RK. J Am Chem Soc 133 20561-20570 (2011)
  29. X-ray crystallographic evidence for the presence of the cysteine tryptophylquinone cofactor in L-lysine ε-oxidase from Marinomonas mediterranea. Okazaki S, Nakano S, Matsui D, Akaji S, Inagaki K, Asano Y. J Biochem 154 233-236 (2013)
  30. Enhanced Rigidification within a Double Mutant of Soybean Lipoxygenase Provides Experimental Support for Vibronically Nonadiabatic Proton-Coupled Electron Transfer Models. Hu S, Soudackov AV, Hammes-Schiffer S, Klinman JP. ACS Catal 7 3569-3574 (2017)
  31. Kinetic isotope effects calculated with the instanton method. Meisner J, Rommel JB, Kästner J. J Comput Chem 32 3456-3463 (2011)
  32. Perspective: Ring-polymer instanton theory. Richardson JO. J Chem Phys 148 200901 (2018)
  33. Chemical accuracy in QM/MM calculations on enzyme-catalysed reactions. Mulholland AJ. Chem Cent J 1 19 (2007)
  34. Mechanisms of reaction in cytochrome P450: Hydroxylation of camphor in P450cam. Zurek J, Foloppe N, Harvey JN, Mulholland AJ. Org Biomol Chem 4 3931-3937 (2006)
  35. Mutagenesis alters the catalytic mechanism of the light-driven enzyme protochlorophyllide oxidoreductase. Menon BR, Davison PA, Hunter CN, Scrutton NS, Heyes DJ. J Biol Chem 285 2113-2119 (2010)
  36. A twin-track approach has optimized proton and hydride transfer by dynamically coupled tunneling during the evolution of protochlorophyllide oxidoreductase. Heyes DJ, Levy C, Sakuma M, Robertson DL, Scrutton NS. J Biol Chem 286 11849-11854 (2011)
  37. An Analysis of All the Relevant Facts and Arguments Indicates that Enzyme Catalysis Does Not Involve Large Contributions from Nuclear Tunneling. Kamerlin SC, Warshel A. J Phys Org Chem 23 677-684 (2010)
  38. Analysis of classical and quantum paths for deprotonation of methylamine by methylamine dehydrogenase. Ranaghan KE, Masgrau L, Scrutton NS, Sutcliffe MJ, Mulholland AJ. Chemphyschem 8 1816-1835 (2007)
  39. MCTDH on-the-fly: Efficient grid-based quantum dynamics without pre-computed potential energy surfaces. Richings GW, Habershon S. J Chem Phys 148 134116 (2018)
  40. Polymorphism and electronic structure of polyimine and its potential significance for prebiotic chemistry on Titan. Rahm M, Lunine JI, Usher DA, Shalloway D. Proc Natl Acad Sci U S A 113 8121-8126 (2016)
  41. Probing quantum and dynamic effects in concerted proton-electron transfer reactions of phenol-base compounds. Markle TF, Tenderholt AL, Mayer JM. J Phys Chem B 116 571-584 (2012)
  42. Solvent effects on environmentally coupled hydrogen tunnelling during catalysis by dihydrofolate reductase from Thermotoga maritima. Loveridge EJ, Evans RM, Allemann RK. Chemistry 14 10782-10788 (2008)
  43. Are environmentally coupled enzymatic hydrogen tunneling reactions influenced by changes in solution viscosity? Hay S, Pudney CR, Sutcliffe MJ, Scrutton NS. Angew Chem Int Ed Engl 47 537-540 (2008)
  44. The chemical mechanism of nitrogenase: hydrogen tunneling and further aspects of the intramolecular mechanism for hydrogenation of eta(2)-N(2) on FeMo-co to NH(3). Dance I. Dalton Trans 5992-5998 (2008)
  45. Tuning of the H-transfer coordinate in primitive versus well-evolved enzymes. Yahashiri A, Howell EE, Kohen A. Chemphyschem 9 980-982 (2008)
  46. Ultrafast infrared spectroscopy reveals water-mediated coherent dynamics in an enzyme active site. Adamczyk K, Simpson N, Greetham GM, Gumiero A, Walsh MA, Towrie M, Parker AW, Hunt NT. Chem Sci 6 505-516 (2015)
  47. Wide-dynamic-range kinetic investigations of deep proton tunnelling in proteins. Salna B, Benabbas A, Sage JT, van Thor J, Champion PM. Nat Chem 8 874-880 (2016)
  48. Enzyme conformational dynamics during catalysis and in the 'resting state' monitored by hydrogen/deuterium exchange mass spectrometry. Liu YH, Konermann L. FEBS Lett 580 5137-5142 (2006)
  49. Cooperative symmetric to asymmetric conformational transition of the apo-form of scavenger decapping enzyme revealed by simulations. Pentikäinen U, Pentikäinen OT, Mulholland AJ. Proteins 70 498-508 (2008)
  50. Deprotonation mechanism of NH4+ in the Escherichia coli ammonium transporter AmtB: insight from QM and QM/MM calculations. Cao Z, Mo Y, Thiel W. Angew Chem Int Ed Engl 46 6811-6815 (2007)
  51. Revealing the subtle interplay of thermal and quantum fluctuation effects on contact ion pairing in microsolvated HCl. Walewski Ł, Forbert H, Marx D. Chemphyschem 14 817-826 (2013)
  52. Solvent as a probe of active site motion and chemistry during the hydrogen tunnelling reaction in morphinone reductase. Hay S, Pudney CR, Sutcliffe MJ, Scrutton NS. Chemphyschem 9 1875-1881 (2008)
  53. Solvent-slaved protein motions accompany proton but not hydride tunneling in light-activated protochlorophyllide oxidoreductase. Heyes DJ, Sakuma M, Scrutton NS. Angew Chem Int Ed Engl 48 3850-3853 (2009)
  54. Substrate polarization in enzyme catalysis: QM/MM analysis of the effect of oxaloacetate polarization on acetyl-CoA enolization in citrate synthase. van der Kamp MW, Perruccio F, Mulholland AJ. Proteins 69 521-535 (2007)
  55. Ab initio QM/MM modelling of acetyl-CoA deprotonation in the enzyme citrate synthase. van der Kamp MW, Perruccio F, Mulholland AJ. J Mol Graph Model 26 676-690 (2007)
  56. Change in heat capacity accurately predicts vibrational coupling in enzyme catalyzed reactions. Arcus VL, Pudney CR. FEBS Lett 589 2200-2206 (2015)
  57. Convergence of theory and experiment on the role of preorganization, quantum tunneling and enzyme motions into flavoenzyme-catalyzed hydride transfer. Delgado M, Görlich S, Longbotham JE, Scrutton NS, Hay S, Moliner V, Tuñón I. ACS Catal 7 3190-3198 (2019)
  58. Interactive chemical reactivity exploration. Haag MP, Vaucher AC, Bosson M, Redon S, Reiher M. Chemphyschem 15 3301-3319 (2014)
  59. Protein Mass Effects on Formate Dehydrogenase. Ranasinghe C, Guo Q, Sapienza PJ, Lee AL, Quinn DM, Cheatum CM, Kohen A. J Am Chem Soc 139 17405-17413 (2017)
  60. Enzymatic reaction sequences as coupled multiple traces on a multidimensional landscape. Swint-Kruse L, Fisher HF. Trends Biochem Sci 33 104-112 (2008)
  61. Hydrogen tunneling in adenosylcobalamin-dependent glutamate mutase: evidence from intrinsic kinetic isotope effects measured by intramolecular competition. Yoon M, Song H, Håkansson K, Marsh EN. Biochemistry 49 3168-3173 (2010)
  62. Nuclear quantum tunnelling in enzymatic reactions--an enzymologist's perspective. Johannissen LO, Hay S, Scrutton NS. Phys Chem Chem Phys 17 30775-30782 (2015)
  63. The enzyme aromatic amine dehydrogenase induces a substrate conformation crucial for promoting vibration that significantly reduces the effective potential energy barrier to proton transfer. Johannissen LO, Scrutton NS, Sutcliffe MJ. J R Soc Interface 5 Suppl 3 S225-32 (2008)
  64. Driving force analysis of proton tunnelling across a reactivity series for an enzyme-substrate complex. Hothi P, Hay S, Roujeinikova A, Sutcliffe MJ, Lee M, Leys D, Cullis PM, Scrutton NS. Chembiochem 9 2839-2845 (2008)
  65. Incorporating Fast Protein Dynamics into Enzyme Design: A Proposed Mutant Aromatic Amine Dehydrogenase. Zoi I, Antoniou D, Schwartz SD. J Phys Chem B 121 7290-7298 (2017)
  66. Exceptional isotopic-substitution effect: breakdown of collective proton tunneling in hexagonal ice due to partial deuteration. Drechsel-Grau C, Marx D. Angew Chem Int Ed Engl 53 10937-10940 (2014)
  67. Intrinsic deuterium kinetic isotope effects in glutamate mutase measured by an intramolecular competition experiment. Yoon M, Kalli A, Lee HY, Håkansson K, Marsh EN. Angew Chem Int Ed Engl 46 8455-8459 (2007)
  68. Quantum mechanical modeling: a tool for the understanding of enzyme reactions. Náray-Szabó G, Oláh J, Krámos B. Biomolecules 3 662-702 (2013)
  69. Significant quantum effects in hydrogen activation. Kyriakou G, Davidson ER, Peng G, Roling LT, Singh S, Boucher MB, Marcinkowski MD, Mavrikakis M, Michaelides A, Sykes EC. ACS Nano 8 4827-4835 (2014)
  70. Computational studies of enzyme mechanism: linking theory with experiment in the analysis of enzymic H-tunnelling. Sutcliffe MJ, Scrutton NS. Phys Chem Chem Phys 8 4510-4516 (2006)
  71. Proton tunnelling and promoting vibrations during the oxidation of ascorbate by ferricyanide? Kandathil SM, Driscoll MD, Dunn RV, Scrutton NS, Hay S. Phys Chem Chem Phys 16 2256-2259 (2014)
  72. Vibrational specificity of proton-transfer dynamics in ground-state tropolone. Murdock D, Burns LA, Vaccaro PH. Phys Chem Chem Phys 12 8285-8299 (2010)
  73. Computer simulations of quantum tunnelling in enzyme-catalysed hydrogen transfer reactions. Ranaghan KE, Mulholland AJ. Interdiscip Sci 2 78-97 (2010)
  74. Crystal structures of AztD provide mechanistic insights into direct zinc transfer between proteins. Neupane DP, Fullam SH, Chacón KN, Yukl ET. Commun Biol 2 308 (2019)
  75. Deep proton tunneling in the electronically adiabatic and non-adiabatic limits: comparison of the quantum and classical treatment of donor-acceptor motion in a protein environment. Benabbas A, Salna B, Sage JT, Champion PM. J Chem Phys 142 114101 (2015)
  76. Spectroscopic characterization of the first ultrafast catalytic intermediate in protochlorophyllide oxidoreductase. Sytina OA, van Stokkum IH, Heyes DJ, Hunter CN, Groot ML. Phys Chem Chem Phys 14 616-625 (2012)
  77. Thermally Induced Intra-Carboxyl Proton Shuttle in a Molecular Rack-and-Pinion Cascade Achieving Macroscopic Crystal Deformation. Huang YG, Shiota Y, Su SQ, Wu SQ, Yao ZS, Li GL, Kanegawa S, Kang S, Kamachi T, Yoshizawa K, Ariga K, Sato O. Angew Chem Int Ed Engl 55 14628-14632 (2016)
  78. Hydride Transfer Mechanism of Enzymatic Sugar Nucleotide C2 Epimerization Probed with a Loose-Fit CDP-Glucose Substrate. Rapp C, Nidetzky B. ACS Catal 12 6816-6830 (2022)
  79. New insights into the reductive half-reaction mechanism of aromatic amine dehydrogenase revealed by reaction with carbinolamine substrates. Roujeinikova A, Hothi P, Masgrau L, Sutcliffe MJ, Scrutton NS, Leys D. J Biol Chem 282 23766-23777 (2007)
  80. Secondary kinetic isotope effects as probes of environmentally-coupled enzymatic hydrogen tunneling reactions. Hay S, Pang J, Monaghan PJ, Wang X, Evans RM, Sutcliffe MJ, Allemann RK, Scrutton NS. Chemphyschem 9 1536-1539 (2008)
  81. Application of high level wavefunction methods in quantum mechanics/molecular mechanics hybrid schemes. Mata RA. Phys Chem Chem Phys 12 5041-5052 (2010)
  82. Collective proton transfer in ordinary ice: local environments, temperature dependence and deuteration effects. Drechsel-Grau C, Marx D. Phys Chem Chem Phys 19 2623-2635 (2017)
  83. Introduction. Biomolecular simulation. Mulholland AJ. J R Soc Interface 5 Suppl 3 S169-72 (2008)
  84. Path integral density matrix dynamics: a method for calculating time-dependent properties in thermal adiabatic and non-adiabatic systems. Habershon S. J Chem Phys 139 104107 (2013)
  85. Structural and Spectroscopic Characterization of a Product Schiff Base Intermediate in the Reaction of the Quinoprotein Glycine Oxidase, GoxA. Avalos D, Sabuncu S, Mamounis KJ, Davidson VL, Moënne-Loccoz P, Yukl ET. Biochemistry 58 706-713 (2019)
  86. The effect of electrostatic shielding on H tunneling in R67 dihydrofolate reductase. Yahashiri A, Nimrod G, Ben-Tal N, Howell EE, Kohen A. Chembiochem 10 2620-2623 (2009)
  87. A computational study of calcium(II) and copper(II) ion binding to the hyaluronate molecule. Pirc ET, Zidar J, Bukovec P. Int J Mol Sci 13 12036-12045 (2012)
  88. Cardiac Contractility Modulation Therapy in Patients with Amyloid Cardiomyopathy and Heart Failure, Case Report, Review of the Biophysics of CCM Function, and AMY-CCM Registry Presentation. Marchese P, Gennaro F, Mazzotta G, Acciarri C, Amabili S, Bonanni C, D'Antonio A, Delfino D, Di Vito L, Partemi M, Pascucci R, Romandini A, Scalone G, Silenzi S, Grossi P. J Clin Med 12 1184 (2023)
  89. Interference of nuclear wavepackets in a pair of proton transfer reactions. Zhang X, Schwarz KN, Zhang L, Fassioli F, Fu B, Nguyen LQ, Knowles RR, Scholes GD. Proc Natl Acad Sci U S A 119 e2212114119 (2022)
  90. Protonation-Initiated Cyclization by a Class II Terpene Cyclase Assisted by Tunneling. Eriksson A, Kürten C, Syrén PO. Chembiochem 18 2301-2305 (2017)
  91. Roles of active-site residues in catalysis, substrate binding, cooperativity, and the reaction mechanism of the quinoprotein glycine oxidase. Mamounis KJ, Yukl ET, Davidson VL. J Biol Chem 295 6472-6481 (2020)
  92. Three applications of path integrals: equilibrium and kinetic isotope effects, and the temperature dependence of the rate constant of the [1,5] sigmatropic hydrogen shift in (Z)-1,3-pentadiene. Zimmermann T, Vaníček J. J Mol Model 16 1779-1787 (2010)
  93. Enthalpic and entropic contributions in the transesterification of sucrose: computational study of lipases and subtilisin. Fuentes G, Ballesteros A, Verma CS. J Biomol Struct Dyn 25 145-155 (2007)
  94. Harmonic oscillators: the quantization of simple systems in the old quantum theory and their functional roles in biology. Steele RH. Mol Cell Biochem 310 19-42 (2008)
  95. New insights into the multi-step reaction pathway of the reductive half-reaction catalysed by aromatic amine dehydrogenase: a QM/MM study. Pang J, Scrutton NS, de Visser SP, Sutcliffe MJ. Chem Commun (Camb) 46 3104-3106 (2010)
  96. The reaction mechanism of Zika virus NS2B/NS3 serine protease inhibition by dipeptidyl aldehyde: a QM/MM study. Nutho B, Mulholland AJ, Rungrotmongkol T. Phys Chem Chem Phys 21 14945-14956 (2019)
  97. Free-Energy Landscape and Proton Transfer Pathways in Oxidative Deamination by Methylamine Dehydrogenase. Zelleke T, Marx D. Chemphyschem 18 208-222 (2017)
  98. Quantum combinatorial model of gene expression. Grover M, Grover R, Singh R, Kumar R, Kumar S. Bioinformation 9 141-144 (2013)
  99. Quantum tunneling time delay investigation of [Formula: see text] ion in human telomeric G-quadruplex systems. Celebi Torabfam G, K Demir G, Demir D. J Biol Inorg Chem 28 213-224 (2023)
  100. Role of water in cyclooxygenase catalysis and design of anti-inflammatory agents targeting two sites of the enzyme. Kaur M, Kaur B, Kaur J, Kaur A, Bhatti R, Singh P. Sci Rep 10 10764 (2020)


Quick links