Probing the remarkable thermal kinetics of visual rhodopsin with E181Q and S186A mutants
Abstract
We recently reported a very unusual temperature dependence of the rate of thermal reaction of wild type bovine rhodopsin: the Arrhenius plot exhibits a sharp “elbow” at 47 °C and, in the upper temperature range, an unexpectedly large activation energy (114 ± 8 kcal/mol) and an enormous prefactor (1072±5 s-1). In this report, we present new measurements and a theoretical model that establish convincingly that this behavior results from a collective, entropy-driven breakup of the rigid hydrogen bonding networks (HBNs) that hinder the reaction at lower temperatures. For E181Q and S186A, two rhodopsin mutants that disrupt the HBNs near the binding pocket of the 11-cis retinyl chromophore, we observe significant decreases in the activation energy (~90 kcal/mol) and prefactor (~1060 s-1), consistent with the conclusion that the reaction rate is enhanced by breakup of the HBN. Finally, the results provide insights into the molecular mechanism of dim-light vision and eye diseases caused by inherited mutations in the rhodopsin gene that perturb the HBNs.
- Authors:
-
- Yale Univ., New Haven, CT (United States). Dept. of Chemistry
- Publication Date:
- Research Org.:
- Yale Univ., New Haven, CT (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)
- OSTI Identifier:
- 1474078
- Alternate Identifier(s):
- OSTI ID: 1365428
- Grant/Contract Number:
- FG02-05ER15677; MCB-0955407; CHE 1465108
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Chemical Physics
- Additional Journal Information:
- Journal Volume: 146; Journal Issue: 21; Journal ID: ISSN 0021-9606
- Publisher:
- American Institute of Physics (AIP)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Guo, Ying, Hendrickson, Heidi P., Videla, Pablo E., Chen, Ya-Na, Ho, Junming, Sekharan, Sivakumar, Batista, Victor S., Tully, John C., and Yan, Elsa C. Y. Probing the remarkable thermal kinetics of visual rhodopsin with E181Q and S186A mutants. United States: N. p., 2017.
Web. doi:10.1063/1.4984818.
Guo, Ying, Hendrickson, Heidi P., Videla, Pablo E., Chen, Ya-Na, Ho, Junming, Sekharan, Sivakumar, Batista, Victor S., Tully, John C., & Yan, Elsa C. Y. Probing the remarkable thermal kinetics of visual rhodopsin with E181Q and S186A mutants. United States. https://doi.org/10.1063/1.4984818
Guo, Ying, Hendrickson, Heidi P., Videla, Pablo E., Chen, Ya-Na, Ho, Junming, Sekharan, Sivakumar, Batista, Victor S., Tully, John C., and Yan, Elsa C. Y. Wed .
"Probing the remarkable thermal kinetics of visual rhodopsin with E181Q and S186A mutants". United States. https://doi.org/10.1063/1.4984818. https://www.osti.gov/servlets/purl/1474078.
@article{osti_1474078,
title = {Probing the remarkable thermal kinetics of visual rhodopsin with E181Q and S186A mutants},
author = {Guo, Ying and Hendrickson, Heidi P. and Videla, Pablo E. and Chen, Ya-Na and Ho, Junming and Sekharan, Sivakumar and Batista, Victor S. and Tully, John C. and Yan, Elsa C. Y.},
abstractNote = {We recently reported a very unusual temperature dependence of the rate of thermal reaction of wild type bovine rhodopsin: the Arrhenius plot exhibits a sharp “elbow” at 47 °C and, in the upper temperature range, an unexpectedly large activation energy (114 ± 8 kcal/mol) and an enormous prefactor (1072±5 s-1). In this report, we present new measurements and a theoretical model that establish convincingly that this behavior results from a collective, entropy-driven breakup of the rigid hydrogen bonding networks (HBNs) that hinder the reaction at lower temperatures. For E181Q and S186A, two rhodopsin mutants that disrupt the HBNs near the binding pocket of the 11-cis retinyl chromophore, we observe significant decreases in the activation energy (~90 kcal/mol) and prefactor (~1060 s-1), consistent with the conclusion that the reaction rate is enhanced by breakup of the HBN. Finally, the results provide insights into the molecular mechanism of dim-light vision and eye diseases caused by inherited mutations in the rhodopsin gene that perturb the HBNs.},
doi = {10.1063/1.4984818},
journal = {Journal of Chemical Physics},
number = 21,
volume = 146,
place = {United States},
year = {Wed Jun 07 00:00:00 EDT 2017},
month = {Wed Jun 07 00:00:00 EDT 2017}
}
Web of Science
Works referenced in this record:
Molecular Mechanisms of Disease for Mutations at Gly-90 in Rhodopsin
journal, September 2011
- Toledo, Darwin; Ramon, Eva; Aguilà, Mònica
- Journal of Biological Chemistry, Vol. 286, Issue 46
Ratio of entropy to enthalpy in thermal transitions in biological tissues
journal, January 2006
- Jacques, Steven L.
- Journal of Biomedical Optics, Vol. 11, Issue 4
Comparison of Stability Predictions and Simulated Unfolding of Rhodopsin Structures†: Photochemistry and Photobiology, 2007, 83
journal, March 2007
- Tastan, Oznur; Yu, Esther; Ganapathiraju, Madhavi
- Photochemistry and Photobiology, Vol. 83, Issue 2
Spectral Tuning of Ultraviolet Cone Pigments: An Interhelical Lock Mechanism
journal, December 2013
- Sekharan, Sivakumar; Mooney, Victoria L.; Rivalta, Ivan
- Journal of the American Chemical Society, Vol. 135, Issue 51
Molecular Mechanisms of Rhodopsin Retinitis Pigmentosa and the Efficacy of Pharmacological Rescue
journal, February 2010
- Krebs, Mark P.; Holden, David C.; Joshi, Parth
- Journal of Molecular Biology, Vol. 395, Issue 5
Relative Stability of Hydrogen and Deuterium Bonds
journal, January 1996
- Scheiner, Steve; Čuma, Martin
- Journal of the American Chemical Society, Vol. 118, Issue 6
Thermal Properties of Rhodopsin: INSIGHT INTO THE MOLECULAR MECHANISM OF DIM-LIGHT VISION
journal, June 2011
- Liu, Jian; Liu, Monica Yun; Nguyen, Jennifer B.
- Journal of Biological Chemistry, Vol. 286, Issue 31
On the molecular origin of photoreceptor noise
journal, November 1993
- Barlow, Robert B.; Birge, Robert R.; Kaplan, Ehud
- Nature, Vol. 366, Issue 6450
Hybrid Models for Combined Quantum Mechanical and Molecular Mechanical Approaches
journal, January 1996
- Bakowies, Dirk; Thiel, Walter
- The Journal of Physical Chemistry, Vol. 100, Issue 25
Stability of Dark State Rhodopsin Is Mediated by a Conserved Ion Pair in Intradiscal Loop E-2
journal, January 2003
- Janz, Jay M.; Fay, Jonathan F.; Farrens, David L.
- Journal of Biological Chemistry, Vol. 278, Issue 19
Entropy–enthalpy compensation of biomolecular systems in aqueous phase: a dry perspective
journal, October 2012
- Movileanu, Liviu; Schiff, Eric A.
- Monatshefte für Chemie - Chemical Monthly, Vol. 144, Issue 1
Influence of surface phase transitions on desorption kinetics: the compensation effect
journal, August 1986
- Estrup, P. J.; Greene, E. F.; Cardillo, M. J.
- The Journal of Physical Chemistry, Vol. 90, Issue 17
A new ONIOM implementation in Gaussian98. Part I. The calculation of energies, gradients, vibrational frequencies and electric field derivatives
journal, April 1999
- Dapprich, Stefan; Komáromi, István; Byun, K. Suzie
- Journal of Molecular Structure: THEOCHEM, Vol. 461-462
Spectral Tuning in Halorhodopsin: The Chloride Pump Photoreceptor
journal, June 2013
- Pal, Rhitankar; Sekharan, Sivakumar; Batista, Victor S.
- Journal of the American Chemical Society, Vol. 135, Issue 26
The Retinal Conformation and its Environment in Rhodopsin in Light of a New 2.2Å Crystal Structure
journal, September 2004
- Okada, Tetsuji; Sugihara, Minoru; Bondar, Ana-Nicoleta
- Journal of Molecular Biology, Vol. 342, Issue 2
The Thermal Stability of Rhodopsin and Opsin
journal, November 1958
- Hubbard, R.
- The Journal of General Physiology, Vol. 42, Issue 2
Origin of the low thermal isomerization rate of rhodopsin chromophore
journal, June 2015
- Yanagawa, Masataka; Kojima, Keiichi; Yamashita, Takahiro
- Scientific Reports, Vol. 5, Issue 1
On the amine-catalyzed isomerization of vitamin A aldehydes
journal, January 1984
- Lukton, David; Rando, Robert R.
- Journal of the American Chemical Society, Vol. 106, Issue 1
Salt Effects on the Conformational Stability of the Visual G-Protein-Coupled Receptor Rhodopsin
journal, December 2011
- Reyes-Alcaraz, Arfaxad; Martínez-Archundia, Marlet; Ramon, Eva
- Biophysical Journal, Vol. 101, Issue 11
Thermal Stability of Rhodopsin and Progression of Retinitis Pigmentosa: COMPARISON OF S186W AND D190N RHODOPSIN MUTANTS
journal, April 2013
- Liu, Monica Yun; Liu, Jian; Mehrotra, Devi
- Journal of Biological Chemistry, Vol. 288, Issue 24
Assessing structural elements that influence Schiff base stability: mutants E113Q and D190N destabilize rhodopsin through different mechanisms
journal, December 2003
- Janz, Jay M.; Farrens, David L.
- Vision Research, Vol. 43, Issue 28
Brownian motion in a field of force and the diffusion model of chemical reactions
journal, April 1940
- Kramers, H. A.
- Physica, Vol. 7, Issue 4
Comparison of the isomerization mechanisms of human melanopsin and invertebrate and vertebrate rhodopsins
journal, January 2014
- Rinaldi, Silvia; Melaccio, Federico; Gozem, Samer
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 5
QM/MM Study of Energy Storage and Molecular Rearrangements Due to the Primary Event in Vision
journal, November 2004
- Gascon, Jose A.; Batista, Victor S.
- Biophysical Journal, Vol. 87, Issue 5
A point mutation of the rhodopsin gene in one form of retinitis pigmentosa
journal, January 1990
- Dryja, Thaddeus P.; McGee, Terri L.; Reichel, Elias
- Nature, Vol. 343, Issue 6256
Why 11- cis -Retinal? Why Not 7- cis -, 9- cis -, or 13- cis- Retinal in the Eye?
journal, November 2011
- Sekharan, Sivakumar; Morokuma, Keiji
- Journal of the American Chemical Society, Vol. 133, Issue 47
Two-state models of protein folding kinetics
journal, January 1997
- Zwanzig, R.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 1
Thermal Decay of Rhodopsin: Role of Hydrogen Bonds in Thermal Isomerization of 11- cis Retinal in the Binding Site and Hydrolysis of Protonated Schiff Base
journal, July 2009
- Liu, Jian; Liu, Monica Yun; Nguyen, Jennifer B.
- Journal of the American Chemical Society, Vol. 131, Issue 25
Unusual kinetics of thermal decay of dim-light photoreceptors in vertebrate vision
journal, July 2014
- Guo, Y.; Sekharan, S.; Liu, J.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 29
IMOMM: A new integratedab initio + molecular mechanics geometry optimization scheme of equilibrium structures and transition states
journal, September 1995
- Maseras, Feliu; Morokuma, Keiji
- Journal of Computational Chemistry, Vol. 16, Issue 9
Reaction-rate theory: fifty years after Kramers
journal, April 1990
- Hänggi, Peter; Talkner, Peter; Borkovec, Michal
- Reviews of Modern Physics, Vol. 62, Issue 2
The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis.
journal, December 1984
- Baylor, D. A.; Nunn, B. J.; Schnapf, J. L.
- The Journal of Physiology, Vol. 357, Issue 1
The Active Site of Melanopsin: The Biological Clock Photoreceptor
journal, November 2012
- Sekharan, Sivakumar; Wei, Jennifer N.; Batista, Victor S.
- Journal of the American Chemical Society, Vol. 134, Issue 48
The Molecular Mechanism of Thermal Noise in Rod Photoreceptors
journal, September 2012
- Gozem, S.; Schapiro, I.; Ferre, N.
- Science, Vol. 337, Issue 6099
Curvature and Hydrophobic Forces Drive Oligomerization and Modulate Activity of Rhodopsin in Membranes
journal, December 2006
- Botelho, Ana Vitória; Huber, Thomas; Sakmar, Thomas P.
- Biophysical Journal, Vol. 91, Issue 12
Quantum Monte Carlo Treatment of the Charge Transfer and Diradical Electronic Character in a Retinal Chromophore Minimal Model
journal, February 2015
- Zen, Andrea; Coccia, Emanuele; Gozem, Samer
- Journal of Chemical Theory and Computation, Vol. 11, Issue 3
Analysis of Disease-Linked Rhodopsin Mutations Based on Structure, Function, and Protein Stability Calculations
journal, January 2011
- Rakoczy, Elizabeth P.; Kiel, Christina; McKeone, Richard
- Journal of Molecular Biology, Vol. 405, Issue 2
Combining Quantum Mechanics Methods with Molecular Mechanics Methods in ONIOM
journal, May 2006
- Vreven, Thom; Byun, K. Suzie; Komáromi, István
- Journal of Chemical Theory and Computation, Vol. 2, Issue 3
Chemical Kinetic Analysis of Thermal Decay of Rhodopsin Reveals Unusual Energetics of Thermal Isomerization and Hydrolysis of Schiff Base
journal, September 2011
- Liu, Jian; Liu, Monica Yun; Fu, Li
- Journal of Biological Chemistry, Vol. 286, Issue 44
Role of the Retinal Hydrogen Bond Network in Rhodopsin Schiff Base Stability and Hydrolysis
journal, October 2004
- Janz, Jay M.; Farrens, David L.
- Journal of Biological Chemistry, Vol. 279, Issue 53
Effects of the Terminal Aromatic Residues on Polyproline Conformation: Thermodynamic and Kinetic Studies
journal, December 2015
- Lin, Yu-Ju; Chu, Li-Kang; Horng, Jia-Cherng
- The Journal of Physical Chemistry B, Vol. 119, Issue 52
Color Vision: “OH-Site” Rule for Seeing Red and Green
journal, June 2012
- Sekharan, Sivakumar; Katayama, Kota; Kandori, Hideki
- Journal of the American Chemical Society, Vol. 134, Issue 25
SORCI for photochemical and thermal reaction paths: A benchmark study
journal, July 2014
- Schapiro, Igor; Neese, Frank
- Computational and Theoretical Chemistry, Vol. 1040-1041
Thermodynamic characterization of the palm tree Roystonea regia peroxidase stability
journal, November 2008
- Zamorano, Laura S.; Pina, David G.; Arellano, Juan B.
- Biochimie, Vol. 90, Issue 11-12
QM/MM Study of Dehydro and Dihydro β-Ionone Retinal Analogues in Squid and Bovine Rhodopsins: Implications for Vision in Salamander Rhodopsin
journal, November 2010
- Sekharan, Sivakumar; Altun, Ahmet; Morokuma, Keiji
- Journal of the American Chemical Society, Vol. 132, Issue 45
QM/MM Study of the Structure, Energy Storage, and Origin of the Bathochromic Shift in Vertebrate and Invertebrate Bathorhodopsins
journal, April 2011
- Sekharan, Sivakumar; Morokuma, Keiji
- Journal of the American Chemical Society, Vol. 133, Issue 13
Structure of Bovine Rhodopsin in a Trigonal Crystal Form
journal, November 2004
- Li, Jade; Edwards, Patricia C.; Burghammer, Manfred
- Journal of Molecular Biology, Vol. 343, Issue 5
Irreversible Denaturation of Maltodextrin Glucosidase Studied by Differential Scanning Calorimetry, Circular Dichroism, and Turbidity Measurements
journal, December 2014
- Goyal, Megha; Chaudhuri, Tapan K.; Kuwajima, Kunihiro
- PLoS ONE, Vol. 9, Issue 12
Structural waters define a functional channel mediating activation of the GPCR, rhodopsin
journal, August 2009
- Angel, T. E.; Gupta, S.; Jastrzebska, B.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 34
Functional role of internal water molecules in rhodopsin revealed by x-ray crystallography
journal, April 2002
- Okada, T.; Fujiyoshi, Y.; Silow, M.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 9
Works referencing / citing this record:
The counterion–retinylidene Schiff base interaction of an invertebrate rhodopsin rearranges upon light activation
journal, May 2019
- Nagata, Takashi; Koyanagi, Mitsumasa; Tsukamoto, Hisao
- Communications Biology, Vol. 2, Issue 1
The counterion–retinylidene Schiff base interaction of an invertebrate rhodopsin rearranges upon light activation
text, January 2019
- Nagata, Takashi; Koyanagi, Mitsumasa; Tsukamoto, Hisao
- ETH Zurich
The counterion–retinylidene Schiff base interaction of an invertebrate rhodopsin rearranges upon light activation
journal, May 2019
- Nagata, Takashi; Koyanagi, Mitsumasa; Tsukamoto, Hisao
- Communications Biology, Vol. 2, Issue 1
Controlling the dynamics of the Nek2 leucine zipper by engineering of "kinetic" disulphide bonds
text, January 2019
- Gutmans, Daniel S.; Whittaker, Sara B-M; Asiani, Karishma
- The Francis Crick Institute