Protein Structural Dynamics of Wild-Type and Mutant Homodimeric Hemoglobin Studied by Time-Resolved X-Ray Solution Scattering

Yang, Cheolhee; Choi, Minseo; Kim, Jong; Kim, Hanui; Muniyappan, Srinivasan; Nozawa, Shunsuke; Adachi, Shin-ichi; Henning, Robert; Kosheleva, Irina; Ihee, Hyotcherl

doi:10.3390/ijms19113633

Protein Structural Dynamics of Wild-Type and Mutant Homodimeric Hemoglobin Studied by Time-Resolved X-Ray Solution Scattering

Journal Article · Thu Nov 01 00:00:00 EDT 2018 · International Journal of Molecular Sciences (Online)

DOI:https://doi.org/10.3390/ijms19113633· OSTI ID:1483878

Yang, Cheolhee; Choi, Minseo; Kim, Jong; Kim, Hanui; Muniyappan, Srinivasan; Nozawa, Shunsuke; Adachi, Shin-ichi; Henning, Robert; Kosheleva, Irina;

The quaternary transition between the relaxed (R) and tense (T) states of heme-binding proteins is a textbook example for the allosteric structural transition. Homodimeric hemoglobin (HbI) from Scapharca inaequivalvis is a useful model system for investigating the allosteric behavior because of the relatively simple quaternary structure. To understand the cooperative transition of HbI, wild-type and mutants of HbI have been studied by using time-resolved X-ray solution scattering (TRXSS), which is sensitive to the conformational changes. Herein, we review the structural dynamics of HbI investigated by TRXSS and compare the results of TRXSS with those of other techniques.

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: DOE - BASIC ENERGY SCIENCESNIH

OSTI ID:: 1483878

Journal Information:: International Journal of Molecular Sciences (Online), Journal Name: International Journal of Molecular Sciences (Online) Journal Issue: 11 Vol. 19; ISSN IJMCFK; ISSN 1422-0067

Publisher:: MDPI

Country of Publication:: United States

Language:: ENGLISH

References (78)

The Short-Lived Signaling State of the Photoactive Yellow Protein Photoreceptor Revealed by Combined Structural Probes Ramachandran, Pradeep L.; Lovett, Janet E.; Carl, Patrick J. Journal of the American Chemical Society, Vol. 133, Issue 24 https://doi.org/10.1021/ja200617t	journal	June 2011
Direct observation of photolysis-induced tertiary structural changes in hemoglobin Adachi, S. -i.; Park, S. -Y.; Tame, J. R. H. Proceedings of the National Academy of Sciences, Vol. 100, Issue 12 https://doi.org/10.1073/pnas.1230629100	journal	May 2003
Direct observation of bond formation in solution with femtosecond X-ray scattering Kim, Kyung Hwan; Kim, Jong Goo; Nozawa, Shunsuke Nature, Vol. 518, Issue 7539 https://doi.org/10.1038/nature14163	journal	February 2015
Ligand Migration and Cavities within Scapharca Dimeric HbI: Studies by Time-Resolved Crystallo- graphy, Xe Binding, and Computational Analysis Knapp, James E.; Pahl, Reinhard; Cohen, Jordi Structure, Vol. 17, Issue 11 https://doi.org/10.1016/j.str.2009.09.004	journal	November 2009
Conformational Substates of Myoglobin Intermediate Resolved by Picosecond X-ray Solution Scattering Oang, Key Young; Kim, Jong Goo; Yang, Cheolhee The Journal of Physical Chemistry Letters, Vol. 5, Issue 5 https://doi.org/10.1021/jz4027425	journal	February 2014
Protein structural dynamics in solution unveiled via 100-ps time-resolved x-ray scattering Cho, H. S.; Dashdorj, N.; Schotte, F. Proceedings of the National Academy of Sciences, Vol. 107, Issue 16 https://doi.org/10.1073/pnas.1002951107	journal	April 2010
Protein Conformational Dynamics of Homodimeric Hemoglobin Revealed by Combined Time-Resolved Spectroscopic Probes Choi, Jungkweon; Muniyappan, Srinivasan; Wallis, John T. ChemPhysChem, Vol. 11, Issue 1 https://doi.org/10.1002/cphc.200900822	journal	January 2010
Structural Analysis of Monomeric Hemichrome and Dimeric Cyanomet Hemoglobins fromCaudina arenicola Mitchell, David T.; Kitto, Barrie G.; Hackert, Marvin L. Journal of Molecular Biology, Vol. 251, Issue 3 https://doi.org/10.1006/jmbi.1995.0445	journal	August 1995
Revisiting the Structure of Hemoglobin and Myoglobin with Cryo-Electron Microscopy Khoshouei, Maryam; Danev, Radostin; Plitzko, Juergen M. Journal of Molecular Biology, Vol. 429, Issue 17 https://doi.org/10.1016/j.jmb.2017.07.004	journal	August 2017
Tracking reaction dynamics in solution by pump–probe X-ray absorption spectroscopy and X-ray liquidography (solution scattering) Kim, Jeongho; Kim, Kyung Hwan; Oang, Key Young Chemical Communications, Vol. 52, Issue 19 https://doi.org/10.1039/C5CC08949B	journal	January 2016
Mutational destabilization of the critical interface water cluster in Scapharca dimeric hemoglobin: structural basis for altered allosteric activity Pardanani, Animesh; Gambacurta, Alessandra; Ascoli, Franca Journal of Molecular Biology, Vol. 284, Issue 3 https://doi.org/10.1006/jmbi.1998.2195	journal	December 1998
Femtosecond X-ray solution scattering reveals that bond formation mechanism of a gold trimer complex is independent of excitation wavelength Kim, Kyung Hwan; Kim, Jong Goo; Oang, Key Young Structural Dynamics, Vol. 3, Issue 4 https://doi.org/10.1063/1.4948516	journal	April 2016
Time-Resolved X-ray Scattering of an Electronically Excited State in Solution. Structure of the ³ A _2u State of Tetrakis-μ-pyrophosphitodiplatinate(II) Christensen, Morten; Haldrup, Kristoffer; Bechgaard, Klaus Journal of the American Chemical Society, Vol. 131, Issue 2 https://doi.org/10.1021/ja804485d	journal	January 2009
Cooperative macromolecular device revealed by meta-analysis of static and time-resolved structures Ren, Z.; Srajer, V.; Knapp, J. E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 1 https://doi.org/10.1073/pnas.1109213108	journal	December 2011
Ligand-Linked Changes at the Subunit Interfaces in Scapharca Hemoglobins Probed through the Sulfhydryl Infrared Absorption ^† Guarrera, Laura; Colotti, Gianni; Chiancone, Emilia Biochemistry, Vol. 38, Issue 31 https://doi.org/10.1021/bi990942k	journal	August 1999
Signal amplification and transduction in phytochrome photosensors Takala, Heikki; Björling, Alexander; Berntsson, Oskar Nature, Vol. 509, Issue 7499 https://doi.org/10.1038/nature13310	journal	April 2014
Rotational dephasing of a gold complex probed by anisotropic femtosecond x-ray solution scattering using an x-ray free-electron laser Kim, Jong Goo; Kim, Kyung Hwan; Oang, Key Young Journal of Physics B: Atomic, Molecular and Optical Physics, Vol. 48, Issue 24 https://doi.org/10.1088/0953-4075/48/24/244005	journal	November 2015
Allosteric action in real time: Time-resolved crystallographic studies of a cooperative dimeric hemoglobin Knapp, J. E.; Pahl, R.; Srajer, V. Proceedings of the National Academy of Sciences, Vol. 103, Issue 20 https://doi.org/10.1073/pnas.0509411103	journal	May 2006
Visualizing Chemical Reactions in Solution by Picosecond X-Ray Diffraction Plech, Anton; Wulff, Michael; Bratos, Savo Physical Review Letters, Vol. 92, Issue 12 https://doi.org/10.1103/PhysRevLett.92.125505	journal	March 2004
Ultrafast myoglobin structural dynamics observed with an X-ray free-electron laser Levantino, Matteo; Schirò, Giorgio; Lemke, Henrik Till Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7772	journal	April 2015
Time-Resolved WAXS Reveals Accelerated Conformational Changes in Iodoretinal-Substituted Proteorhodopsin Malmerberg, Erik; Omran, Ziad; Hub, Jochen S. Biophysical Journal, Vol. 101, Issue 6 https://doi.org/10.1016/j.bpj.2011.07.050	journal	September 2011
Proximal and Distal Effects on the Coordination Chemistry of Ferric Scapharca Homodimeric Hemoglobin As Revealed by Heme Pocket Mutants ^† Boffi, Alberto; Guarrera, Laura; Giangiacomo, Laura Biochemistry, Vol. 39, Issue 12 https://doi.org/10.1021/bi9923003	journal	March 2000
Protein Tertiary Structural Changes Visualized by Time-Resolved X-ray Solution Scattering Ahn, Sena; Kim, Kyung Hwan; Kim, Youngmin The Journal of Physical Chemistry B, Vol. 113, Issue 40 https://doi.org/10.1021/jp906983v	journal	October 2009
Pump-Probe X-ray Solution Scattering Reveals Accelerated Folding of Cytochrome c Upon Suppression of Misligation Kim, Tae Wu; Kim, Jong Goo; Yang, Cheolhee Bulletin of the Korean Chemical Society, Vol. 35, Issue 3 https://doi.org/10.5012/bkcs.2014.35.3.697	journal	March 2014
Stereochemistry of Cooperative Effects in Haemoglobin: Haem–Haem Interaction and the Problem of Allostery Perutz, M. F. Nature, Vol. 228, Issue 5273 https://doi.org/10.1038/228726a0	journal	November 1970
An Optical Signal Correlated with the Allosteric Transition in Scapharca inaequivalvis HbI ^† Nichols, Jeffry C.; Royer,, William E.; Gibson, Quentin H. Biochemistry, Vol. 45, Issue 51 https://doi.org/10.1021/bi061451k	journal	December 2006
Anisotropic Picosecond X-ray Solution Scattering from Photoselectively Aligned Protein Molecules Kim, Jeongho; Kim, Kyung Hwan; Kim, Jong Goo The Journal of Physical Chemistry Letters, Vol. 2, Issue 5 https://doi.org/10.1021/jz101503r	journal	February 2011
Combined probes of X-ray scattering and optical spectroscopy reveal how global conformational change is temporally and spatially linked to local structural perturbation in photoactive yellow protein Kim, Tae Wu; Yang, Cheolhee; Kim, Youngmin Physical Chemistry Chemical Physics, Vol. 18, Issue 13 https://doi.org/10.1039/C6CP00476H	journal	January 2016
Sub-100-ps structural dynamics of horse heart myoglobin probed by time-resolved X-ray solution scattering Oang, Key Young; Kim, Kyung Hwan; Jo, Junbeom Chemical Physics, Vol. 442 https://doi.org/10.1016/j.chemphys.2014.03.004	journal	October 2014
Structure of human oxyhaemoglobin at 2·1resolution Shaanan, Boaz Journal of Molecular Biology, Vol. 171, Issue 1 https://doi.org/10.1016/S0022-2836(83)80313-1	journal	November 1983
Ultrafast X-ray Solution Scattering Reveals Different Reaction Pathways in the Photolysis of Triruthenium Dodecacarbonyl (Ru ₃ (CO) ₁₂ ) after Ultraviolet and Visible Excitation Kong, Qingyu; Lee, Jae Hyuk; Kim, Kyung Hwan Journal of the American Chemical Society, Vol. 132, Issue 8 https://doi.org/10.1021/ja9097548	journal	March 2010
Structural transitions upon ligand binding in a cooperative dimeric hemoglobin Royer, W.; Hendrickson, W.; Chiancone, E. Science, Vol. 249, Issue 4968 https://doi.org/10.1126/science.2382132	journal	August 1990
Structural Dynamics of 1,2-Diiodoethane in Cyclohexane Probed by Picosecond X-ray Liquidography Kim, Jeongho; Lee, Jae Hyuk; Kim, Joonghan The Journal of Physical Chemistry A, Vol. 116, Issue 11 https://doi.org/10.1021/jp2078314	journal	December 2011
Communication maps computed for homodimeric hemoglobin: Computational study of water-mediated energy transport in proteins Gnanasekaran, Ramachandran; Agbo, Johnson K.; Leitner, David M. The Journal of Chemical Physics, Vol. 135, Issue 6 https://doi.org/10.1063/1.3623423	journal	August 2011
The Apolar Distal Histidine Mutant (His69→Val) of the Homodimeric Scapharca Hemoglobin Is in an R -like Conformation ^† Guarrera, Laura; Colotti, Gianni; Boffi, Alberto Biochemistry, Vol. 37, Issue 16 https://doi.org/10.1021/bi972380f	journal	April 1998
Bacterial Expression Of Scapharca Dimeric Hemoglobin: A Simple Model System For Investigating Protein Cooperativity Summerford, Candace M.; Pardanani, Animesh; Betts, Andrew H. "Protein Engineering, Design and Selection", Vol. 8, Issue 6 https://doi.org/10.1093/protein/8.6.593	journal	January 1995
Lumbricus Erythrocruorin at 3.5 Å Resolution: Architecture of a Megadalton Respiratory Complex Royer, William E.; Sharma, Hitesh; Strand, Kristen Structure, Vol. 14, Issue 7 https://doi.org/10.1016/j.str.2006.05.011	journal	July 2006
Direct Observation of a Transiently Formed Isomer During Iodoform Photolysis in Solution by Time-Resolved X-ray Liquidography Ahn, Chi Woo; Ki, Hosung; Kim, Joonghan The Journal of Physical Chemistry Letters, Vol. 9, Issue 3 https://doi.org/10.1021/acs.jpclett.7b03125	journal	January 2018
Visualizing Solution-Phase Reaction Dynamics with Time-Resolved X-ray Liquidography Ihee, Hyotcherl Accounts of Chemical Research, Vol. 42, Issue 2 https://doi.org/10.1021/ar800168v	journal	February 2009
Time-Resolved Small-Angle X-ray Scattering Study of the Folding Dynamics of Barnase Konuma, Tsuyoshi; Kimura, Tetsunari; Matsumoto, Shuzo Journal of Molecular Biology, Vol. 405, Issue 5 https://doi.org/10.1016/j.jmb.2010.11.052	journal	February 2011
Ordered water molecules as key allosteric mediators in a cooperative dimeric hemoglobin Royer, W. E.; Pardanani, A.; Gibson, Q. H. Proceedings of the National Academy of Sciences, Vol. 93, Issue 25 https://doi.org/10.1073/pnas.93.25.14526	journal	December 1996
Direct observation of myoglobin structural dynamics from 100 picoseconds to 1 microsecond with picosecond X-ray solution scattering Kim, Kyung Hwan; Oang, Key Young; Kim, Jeongho Chem. Commun., Vol. 47, Issue 1 https://doi.org/10.1039/C0CC01817A	journal	January 2011
SVD-aided pseudo principal-component analysis: A new method to speed up and improve determination of the optimum kinetic model from time-resolved data Oang, Key Young; Yang, Cheolhee; Muniyappan, Srinivasan Structural Dynamics, Vol. 4, Issue 4 https://doi.org/10.1063/1.4979854	journal	July 2017
Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser Arnlund, David; Johansson, Linda C.; Wickstrand, Cecilia Nature Methods, Vol. 11, Issue 9 https://doi.org/10.1038/nmeth.3067	journal	August 2014
Identifying the major intermediate species by combining time-resolved X-ray solution scattering and X-ray absorption spectroscopy Kim, Kyung Hwan; Kim, Jeongho; Oang, Key Young Physical Chemistry Chemical Physics, Vol. 17, Issue 36 https://doi.org/10.1039/C5CP03686K	journal	January 2015
Cooperative protein structural dynamics of homodimeric hemoglobin linked to water cluster at subunit interface revealed by time-resolved X-ray solution scattering Kim, Jong Goo; Muniyappan, Srinivasan; Oang, Key Young Structural Dynamics, Vol. 3, Issue 2 https://doi.org/10.1063/1.4947071	journal	March 2016
Cooperative hemoglobins: conserved fold, diverse quaternary assemblies and allosteric mechanisms Royer, William E.; Knapp, James E.; Strand, Kristen Trends in Biochemical Sciences, Vol. 26, Issue 5 https://doi.org/10.1016/S0968-0004(01)01811-4	journal	May 2001
Haemoglobin: The structural changes related to ligand binding and its allosteric mechanism Baldwin, Joyce; Chothia, Cyrus Journal of Molecular Biology, Vol. 129, Issue 2 https://doi.org/10.1016/0022-2836(79)90277-8	journal	April 1979
Atomistic characterization of the active-site solvation dynamics of a model photocatalyst van Driel, Tim B.; Kjær, Kasper S.; Hartsock, Robert W. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13678	journal	November 2016
Denaturation of a Protein Monitored by Diffusion Coefficients: Myoglobin Choi, Jungkwon; Terazima, Masahide The Journal of Physical Chemistry B, Vol. 106, Issue 25 https://doi.org/10.1021/jp0256802	journal	June 2002
Ultrafast X-Ray Crystallography and Liquidography Ki, Hosung; Oang, Key Young; Kim, Jeongho Annual Review of Physical Chemistry, Vol. 68, Issue 1 https://doi.org/10.1146/annurev-physchem-052516-050851	journal	May 2017
Cooperativity in Scapharca Dimeric Hemoglobin: Simulation of Binding Intermediates and Elucidation of the Role of Interfacial Water Zhou, Yaoqi; Zhou, Hongyi; Karplus, Martin Journal of Molecular Biology, Vol. 326, Issue 2 https://doi.org/10.1016/S0022-2836(02)01329-3	journal	February 2003
Insight into the Allosteric Mechanism of Scapharca Dimeric Hemoglobin Laine, Jennifer M.; Amat, Miguel; Morgan, Brittany R. Biochemistry, Vol. 53, Issue 46 https://doi.org/10.1021/bi500591s	journal	November 2014
High-Resolution Crystallographic Analysis of a Co-operative Dimeric Hemoglobin Royer, William E. Journal of Molecular Biology, Vol. 235, Issue 2 https://doi.org/10.1006/jmbi.1994.1019	journal	January 1994
Residue F4 Plays a Key Role in Modulating Oxygen Affinity and Cooperativity in Scapharca Dimeric Hemoglobin Knapp, James E.; Bonham, Michele A.; Gibson, Quentin H. Biochemistry, Vol. 44, Issue 44 https://doi.org/10.1021/bi051052+	journal	October 2005
Mechanisms of cooperativity and allosteric regulation in proteins Perutz, M. F. Quarterly Reviews of Biophysics, Vol. 22, Issue 2 https://doi.org/10.1017/S0033583500003826	journal	May 1989
Time-resolved Absorption and UV Resonance Raman Spectra Reveal Stepwise Formation of T Quaternary Contacts in the Allosteric Pathway of Hemoglobin Balakrishnan, Gurusamy; Case, Martin A.; Pevsner, Alex Journal of Molecular Biology, Vol. 340, Issue 4 https://doi.org/10.1016/j.jmb.2004.05.012	journal	July 2004
Nanosecond dynamics of the R-->T transition in hemoglobin: ultraviolet Raman studies Rodgers, K.; Spiro, T. Science, Vol. 265, Issue 5179 https://doi.org/10.1126/science.8085153	journal	September 1994
On the nature of allosteric transitions: A plausible model Monod, Jacque; Wyman, Jeffries; Changeux, Jean-Pierre Journal of Molecular Biology, Vol. 12, Issue 1 https://doi.org/10.1016/S0022-2836(65)80285-6	journal	May 1965
Ligand-Linked Structural Transitions in Crystals of a Cooperative Dimeric Hemoglobin ^† Knapp, James E.; Royer, William E. Biochemistry, Vol. 42, Issue 16 https://doi.org/10.1021/bi027136p	journal	April 2003
Mutation of Residue Phe ⁹⁷ to Leu Disrupts the Central Allosteric Pathway in Scapharca Dimeric Hemoglobin Pardanani, Animesh; Gibson, Quentin H.; Colotti, Gianni Journal of Biological Chemistry, Vol. 272, Issue 20 https://doi.org/10.1074/jbc.272.20.13171	journal	May 1997
Dynamics of Water Clusters Confined in Proteins: A Molecular Dynamics Simulation Study of Interfacial Waters in a Dimeric Hemoglobin Gnanasekaran, Ramachandran; Xu, Yao; Leitner, David M. The Journal of Physical Chemistry B, Vol. 114, Issue 50 https://doi.org/10.1021/jp109173t	journal	December 2010
Protein Structural Dynamics of Photoactive Yellow Protein in Solution Revealed by Pump–Probe X-ray Solution Scattering Kim, Tae Wu; Lee, Jae Hyuk; Choi, Jungkweon Journal of the American Chemical Society, Vol. 134, Issue 6 https://doi.org/10.1021/ja210435n	journal	February 2012
A practical guide to small angle X-ray scattering (SAXS) of flexible and intrinsically disordered proteins Kikhney, Alexey G.; Svergun, Dmitri I. FEBS Letters, Vol. 589, Issue 19PartA https://doi.org/10.1016/j.febslet.2015.08.027	journal	August 2015
Cooperative Oxygen Binding to Scapharca inaequivalvis Hemoglobin in the Crystal Mozzarelli, Andrea; Bettati, Stefano; Rivetti, Claudio Journal of Biological Chemistry, Vol. 271, Issue 7 https://doi.org/10.1074/jbc.271.7.3627	journal	February 1996
Tracking the structural dynamics of proteins in solution using time-resolved wide-angle X-ray scattering Cammarata, Marco; Levantino, Matteo; Schotte, Friedrich Nature Methods, Vol. 5, Issue 10 https://doi.org/10.1038/nmeth.1255	journal	September 2008
Cryo-EM structure of haemoglobin at 3.2 Å determined with the Volta phase plate Khoshouei, Maryam; Radjainia, Mazdak; Baumeister, Wolfgang Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms16099	journal	June 2017
Ligand Migration and Binding in the Dimeric Hemoglobin of Scapharca inaequivalvis ^† ^, ^‡ Nienhaus, Karin; Knapp, James E.; Palladino, Pasquale Biochemistry, Vol. 46, Issue 49 https://doi.org/10.1021/bi7016798	journal	December 2007
Restricting the Ligand-Linked Heme Movement in Scapharca Dimeric Hemoglobin Reveals Tight Coupling between Distal and Proximal Contributions to Cooperativity ^† Knapp, James E.; Gibson, Quentin H.; Cushing, Lauren Biochemistry, Vol. 40, Issue 49 https://doi.org/10.1021/bi011071t	journal	December 2001
Structural Dynamics of Light-Driven Proton Pumps Andersson, Magnus; Malmerberg, Erik; Westenhoff, Sebastian Structure, Vol. 17, Issue 9 https://doi.org/10.1016/j.str.2009.07.007	journal	September 2009
Dimeric and tetrameric hemoglobins from the mollusc Scapharca inaequivalvis Chiancone, Emilia; Vecchini, Paola; Verzili, Daniela Journal of Molecular Biology, Vol. 152, Issue 3 https://doi.org/10.1016/0022-2836(81)90270-9	journal	November 1981
Hemoglobin allostery: resonance Raman spectroscopy of kinetic intermediates Jayaraman, V.; Rodgers, K.; Mukerji, I. Science, Vol. 269, Issue 5232 https://doi.org/10.1126/science.7569921	journal	September 1995
Ultrafast X-ray Diffraction of Transient Molecular Structures in Solution Ihee, H. Science, Vol. 309, Issue 5738 https://doi.org/10.1126/science.1114782	journal	August 2005
Transient X-ray Diffraction Reveals Global and Major Reaction Pathways for the Photolysis of Iodoform in Solution Lee, Jae Hyuk; Kim, Joonghan; Cammarata, Marco Angewandte Chemie International Edition, Vol. 47, Issue 6 https://doi.org/10.1002/anie.200704150	journal	January 2008
Unveiling the Timescale of the R–T Transition in Human Hemoglobin Cammarata, M.; Levantino, M.; Wulff, M. Journal of Molecular Biology, Vol. 400, Issue 5 https://doi.org/10.1016/j.jmb.2010.05.057	journal	July 2010
Solvent dependent structural perturbations of chemical reaction intermediates visualized by time-resolved x-ray diffraction Vincent, Jonathan; Andersson, Magnus; Eklund, Mattias The Journal of Chemical Physics, Vol. 130, Issue 15 https://doi.org/10.1063/1.3111401	journal	April 2009
Direct Observation of Cooperative Protein Structural Dynamics of Homodimeric Hemoglobin from 100 ps to 10 ms with Pump–Probe X-ray Solution Scattering Kim, Kyung Hwan; Muniyappan, Srinivasan; Oang, Key Young Journal of the American Chemical Society, Vol. 134, Issue 16 https://doi.org/10.1021/ja210856v	journal	April 2012
The crystal structure of human deoxyhaemoglobin at 1.74 Å resolution Fermi, G.; Perutz, M. F.; Shaanan, B. Journal of Molecular Biology, Vol. 175, Issue 2 https://doi.org/10.1016/0022-2836(84)90472-8	journal	May 1984

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