Structural Coupling Throughout the Active Site Hydrogen Bond Networks of Ketosteroid Isomerase and Photoactive Yellow Protein

Pinney, Margaux M.; Natarajan, Aditya; Yabukarski, Filip; Sanchez, David M.; Liu, Fang; Liang, Ruibin; Doukov, Tzanko; Schwans, Jason P.; Martinez, Todd J.; Herschlag, Daniel

doi:10.1021/jacs.8b01596

Title: Structural Coupling Throughout the Active Site Hydrogen Bond Networks of Ketosteroid Isomerase and Photoactive Yellow Protein

Journal Article · Tue Jul 10 00:00:00 EDT 2018 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.8b01596· OSTI ID:1476146

^[1]; Natarajan, Aditya ^[1]; Yabukarski, Filip ^[1]; Sanchez, David M. ^[2];

^[3];

^[2]; Doukov, Tzanko ^[4]; Schwans, Jason P. ^[5];

^[2];

^[1]

Stanford Univ., Stanford, CA (United States)
Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Stanford Univ., Stanford, CA (United States); California State Univ. Long Beach, Long Beach, CA (United States)

Hydrogen bonds are fundamental to biological systems and are regularly found in networks implicated in folding, molecular recognition, catalysis, and allostery. Given their ubiquity, we asked the fundamental questions of whether, and to what extent, hydrogen bonds within networks are structurally coupled. To address these questions, we turned to three protein systems, two variants of ketosteroid isomerase and one of photoactive yellow protein. We perturbed their hydrogen bond networks via a combination of site-directed mutagenesis and unnatural amino acid substitution, and we used ¹H NMR and high-resolution X-ray crystallography to determine the effects of these perturbations on the lengths of the two oxyanion hole hydrogen bonds that are donated to negatively charged transition state analogs. Perturbations that lengthened or shortened one of the oxyanion hole hydrogen bonds had the opposite effect on the other. The oxyanion hole hydrogen bonds were also affected by distal hydrogen bonds in the network, with smaller perturbations for more remote hydrogen bonds. Across 19 measurements in three systems, the length change in one oxyanion hole hydrogen bond was propagated to the other, by a factor of –0.30 ± 0.03. This common effect suggests that hydrogen bond coupling is minimally influenced by the remaining protein scaffold. The observed coupling is reproduced by molecular mechanics and quantum mechanics/molecular mechanics (QM/MM) calculations for changes to a proximal oxyanion hole hydrogen bond. However, effects from distal hydrogen bonds are reproduced only by QM/MM, suggesting the importance of polarization in hydrogen bond coupling. These results deepen our understanding of hydrogen bonds and their networks, providing strong evidence for long-range coupling and for the extent of this coupling. In conclusion, we provide a broadly predictive quantitative relationship that can be applied to and can be further tested in new systems.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-76SF00515; MCB-1714723

OSTI ID:: 1476146

Journal Information:: Journal of the American Chemical Society, Vol. 140, Issue 31; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 29 works

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Ab Initio Quantum Chemistry for Protein Structures Kulik, Heather J.; Luehr, Nathan; Ufimtsev, Ivan S. The Journal of Physical Chemistry B, Vol. 116, Issue 41 https://doi.org/10.1021/jp307741u	journal	October 2012
Solvent-Induced Red-Shifts for the Proton Stretch Vibrational Frequency in a Hydrogen-Bonded Complex. 1. A Valence Bond-Based Theoretical Approach Kiefer, Philip M.; Pines, Ehud; Pines, Dina The Journal of Physical Chemistry B, Vol. 118, Issue 28 https://doi.org/10.1021/jp501815j	journal	May 2014
Microscopic rate constants for the acetate ion catalyzed isomerization of 5-androstene-3,17-dione to 4-androstene-3,17-dione: a model for steroid isomerase Zeng, Baifei; Pollack, Ralph M. Journal of the American Chemical Society, Vol. 113, Issue 10 https://doi.org/10.1021/ja00010a028	journal	May 1991
Evaluation of the Catalytic Contribution from a Positioned General Base in Ketosteroid Isomerase Lamba, Vandana; Yabukarski, Filip; Pinney, Margaux Journal of the American Chemical Society, Vol. 138, Issue 31 https://doi.org/10.1021/jacs.6b04796	journal	July 2016
Dissecting the paradoxical effects of hydrogen bond mutations in the ketosteroid isomerase oxyanion hole Kraut, D. A.; Sigala, P. A.; Fenn, T. D. Proceedings of the National Academy of Sciences, Vol. 107, Issue 5 https://doi.org/10.1073/pnas.0911168107	journal	January 2010
Reaction Pathways of Proton Transfer in Hydrogen-Bonded Phenol–Carboxylate Complexes Explored by Combined UV–Vis and NMR Spectroscopy Koeppe, Benjamin; Tolstoy, Peter M.; Limbach, Hans-Heinrich Journal of the American Chemical Society, Vol. 133, Issue 20 https://doi.org/10.1021/ja201113a	journal	May 2011
Electrophilic Assistance by Asp-99 of 3-Oxo-Δ ⁵ -steroid Isomerase Thornburg, Lora D.; Hénot, Frédéric; Bash, Diarmad P. Biochemistry, Vol. 37, Issue 29 https://doi.org/10.1021/bi980099a	journal	June 1998

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Symmetry and ¹ H NMR chemical shifts of short hydrogen bonds: impact of electronic and nuclear quantum effects Zhou, Shengmin; Wang, Lu Physical Chemistry Chemical Physics, Vol. 22, Issue 9 https://doi.org/10.1039/c9cp06840f	journal	January 2020
Assessment of enzyme active site positioning and tests of catalytic mechanisms through X-ray–derived conformational ensembles Yabukarski, Filip; Biel, Justin T.; Pinney, Margaux M. Proceedings of the National Academy of Sciences, Vol. 117, Issue 52 https://doi.org/10.1073/pnas.2011350117	journal	December 2020

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