Cooperative protein structural dynamics of homodimeric hemoglobin linked to water cluster at subunit interface revealed by time-resolved X-ray solution scattering
Abstract
Homodimeric hemoglobin (HbI) consisting of two subunits is a good model system for investigating the allosteric structural transition as it exhibits cooperativity in ligand binding. In this work, as an effort to extend our previous study on wild-type and F97Y mutant HbI, we investigate structural dynamics of a mutant HbI in solution to examine the role of well-organized interfacial water cluster, which has been known to mediate intersubunit communication in HbI. In the T72V mutant of HbI, the interfacial water cluster in the T state is perturbed due to the lack of Thr72, resulting in two less interfacial water molecules than in wild-type HbI. By performing picosecond time-resolved X-ray solution scattering experiment and kinetic analysis on the T72V mutant, we identify three structurally distinct intermediates (I1, I2, and I3) and show that the kinetics of the T72V mutant are well described by the same kinetic model used for wild-type and F97Y HbI, which involves biphasic kinetics, geminate recombination, and bimolecular CO recombination. The optimized kinetic model shows that the R-T transition and bimolecular CO recombination are faster in the T72V mutant than in the wild type. From structural analysis using species-associated difference scattering curves for the intermediates, we find thatmore »
- Authors:
-
- KAIST, Daejeon (South Korea); Inst. for Basic Science (IBS), Daejeon (South Korea)
- Inha Univ., Incheon (South Korea)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Research Foundation of Korea (NRF); NIH National Inst. of General Medical Sciences
- OSTI Identifier:
- 1248391
- Grant/Contract Number:
- AC02-06CH11357; NRF-2014R1A1A1002511; R24GM111072
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Structural Dynamics
- Additional Journal Information:
- Journal Volume: 3; Journal Issue: 2; Journal ID: ISSN 2329-7778
- Publisher:
- American Crystallographic Association/AIP
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Kim, Jong Goo, Muniyappan, Srinivasan, Oang, Key Young, Kim, Tae Wu, Yang, Cheolhee, Kim, Kyung Hwan, Kim, Jeongho, and Ihee, Hyotcherl. Cooperative protein structural dynamics of homodimeric hemoglobin linked to water cluster at subunit interface revealed by time-resolved X-ray solution scattering. United States: N. p., 2016.
Web. doi:10.1063/1.4947071.
Kim, Jong Goo, Muniyappan, Srinivasan, Oang, Key Young, Kim, Tae Wu, Yang, Cheolhee, Kim, Kyung Hwan, Kim, Jeongho, & Ihee, Hyotcherl. Cooperative protein structural dynamics of homodimeric hemoglobin linked to water cluster at subunit interface revealed by time-resolved X-ray solution scattering. United States. https://doi.org/10.1063/1.4947071
Kim, Jong Goo, Muniyappan, Srinivasan, Oang, Key Young, Kim, Tae Wu, Yang, Cheolhee, Kim, Kyung Hwan, Kim, Jeongho, and Ihee, Hyotcherl. 2016.
"Cooperative protein structural dynamics of homodimeric hemoglobin linked to water cluster at subunit interface revealed by time-resolved X-ray solution scattering". United States. https://doi.org/10.1063/1.4947071. https://www.osti.gov/servlets/purl/1248391.
@article{osti_1248391,
title = {Cooperative protein structural dynamics of homodimeric hemoglobin linked to water cluster at subunit interface revealed by time-resolved X-ray solution scattering},
author = {Kim, Jong Goo and Muniyappan, Srinivasan and Oang, Key Young and Kim, Tae Wu and Yang, Cheolhee and Kim, Kyung Hwan and Kim, Jeongho and Ihee, Hyotcherl},
abstractNote = {Homodimeric hemoglobin (HbI) consisting of two subunits is a good model system for investigating the allosteric structural transition as it exhibits cooperativity in ligand binding. In this work, as an effort to extend our previous study on wild-type and F97Y mutant HbI, we investigate structural dynamics of a mutant HbI in solution to examine the role of well-organized interfacial water cluster, which has been known to mediate intersubunit communication in HbI. In the T72V mutant of HbI, the interfacial water cluster in the T state is perturbed due to the lack of Thr72, resulting in two less interfacial water molecules than in wild-type HbI. By performing picosecond time-resolved X-ray solution scattering experiment and kinetic analysis on the T72V mutant, we identify three structurally distinct intermediates (I1, I2, and I3) and show that the kinetics of the T72V mutant are well described by the same kinetic model used for wild-type and F97Y HbI, which involves biphasic kinetics, geminate recombination, and bimolecular CO recombination. The optimized kinetic model shows that the R-T transition and bimolecular CO recombination are faster in the T72V mutant than in the wild type. From structural analysis using species-associated difference scattering curves for the intermediates, we find that the T-like deoxy I3 intermediate in solution has a different structure from deoxy HbI in crystal. In addition, we extract detailed structural parameters of the intermediates such as E-F distance, intersubunit rotation angle, and heme-heme distance. By comparing the structures of protein intermediates in wild-type HbI and the T72V mutant, we reveal how the perturbation in the interfacial water cluster affects the kinetics and structures of reaction intermediates of HbI.},
doi = {10.1063/1.4947071},
url = {https://www.osti.gov/biblio/1248391},
journal = {Structural Dynamics},
issn = {2329-7778},
number = 2,
volume = 3,
place = {United States},
year = {Thu Apr 14 00:00:00 EDT 2016},
month = {Thu Apr 14 00:00:00 EDT 2016}
}
Web of Science
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