1gzx Citations

Crystal structure of T state haemoglobin with oxygen bound at all four haems.

J Mol Biol 256 775-92 (1996)
Cited: 106 times
EuropePMC logo PMID: 8642597

Abstract

The cooperative binding of oxygen by haemoglobin results from restraints on ligand binding in the T state. The unfavourable interactions made by the ligands at the haems destabilise the T state and favour the high affinity R state. The T <==> R equilibrium leads, in the presence of a ligand, to a rapid increase in the R state population and therefore generates cooperative binding. There is now considerable understanding of this phenomenon, but the interactions that reduce ligand affinity in the T state have not yet been fully explored, owing to the difficulties in preparing T state haemoglobin crystals in which all the subunits are oxygenated. A protocol has been developed to oxygenate deoxy T state adult human haemoglobin (HbA) crystals in air at 4 C at all four haems without significant loss of crystalline order. The X-ray crystal structure, determined to 2.1 A spacing, shows significant changes in the alpha and beta haem pockets as well as changes at the alpha(1)beta(2) interface in the direction of the R quaternary structure. Most of the shifts and deviations from deoxy T state HbA are similar to, but larger than, those previously observed in the T state met and other partially liganded T state forms. They provide clear evidence of haem-haem interaction in the T state.

Reviews - 1gzx mentioned but not cited (4)

  1. The ensemble nature of allostery. Motlagh HN, Wrabl JO, Li J, Hilser VJ. Nature 508 331-339 (2014)
  2. Immunological properties of oxygen-transport proteins: hemoglobin, hemocyanin and hemerythrin. Coates CJ, Decker H. Cell Mol Life Sci 74 293-317 (2017)
  3. Lessons from Nature: A Bio-Inspired Approach to Molecular Design. Cook SA, Hill EA, Borovik AS. Biochemistry 54 4167-4180 (2015)
  4. A Glimpse to Background and Characteristics of Major Molecular Biological Networks. Altaf-Ul-Amin M, Katsuragi T, Sato T, Kanaya S. Biomed Res Int 2015 540297 (2015)

Articles - 1gzx mentioned but not cited (34)

  1. EzMol: A Web Server Wizard for the Rapid Visualization and Image Production of Protein and Nucleic Acid Structures. Reynolds CR, Islam SA, Sternberg MJE. J Mol Biol 430 2244-2248 (2018)
  2. The implementation of SOMO (SOlution MOdeller) in the UltraScan analytical ultracentrifugation data analysis suite: enhanced capabilities allow the reliable hydrodynamic modeling of virtually any kind of biomacromolecule. Brookes E, Demeler B, Rosano C, Rocco M. Eur Biophys J 39 423-435 (2010)
  3. Structural basis for hemoglobin capture by Staphylococcus aureus cell-surface protein, IsdH. Krishna Kumar K, Jacques DA, Pishchany G, Caradoc-Davies T, Spirig T, Malmirchegini GR, Langley DB, Dickson CF, Mackay JP, Clubb RT, Skaar EP, Guss JM, Gell DA. J Biol Chem 286 38439-38447 (2011)
  4. Spontaneous quaternary and tertiary T-R transitions of human hemoglobin in molecular dynamics simulation. Hub JS, Kubitzki MB, de Groot BL. PLoS Comput Biol 6 e1000774 (2010)
  5. Evolutionary trace annotation of protein function in the structural proteome. Erdin S, Ward RM, Venner E, Lichtarge O. J Mol Biol 396 1451-1473 (2010)
  6. Predicting Protein Complex Structure from Surface-Induced Dissociation Mass Spectrometry Data. Seffernick JT, Harvey SR, Wysocki VH, Lindert S. ACS Cent Sci 5 1330-1341 (2019)
  7. Peroxide Activation Regulated by Hydrogen Bonds within Artificial Cu Proteins. Mann SI, Heinisch T, Ward TR, Borovik AS. J Am Chem Soc 139 17289-17292 (2017)
  8. Kinetics of α-globin binding to α-hemoglobin stabilizing protein (AHSP) indicate preferential stabilization of hemichrome folding intermediate. Mollan TL, Khandros E, Weiss MJ, Olson JS. J Biol Chem 287 11338-11350 (2012)
  9. Methemoglobin Formation and Characterization of Hemoglobin Adducts of Carcinogenic Aromatic Amines and Heterocyclic Aromatic Amines. Pathak KV, Chiu TL, Amin EA, Turesky RJ. Chem Res Toxicol 29 255-269 (2016)
  10. Complex nature of malaria parasite hemoglobin degradation [corrected]. Goldberg DE. Proc Natl Acad Sci U S A 110 5283-5284 (2013)
  11. A cis-proline in alpha-hemoglobin stabilizing protein directs the structural reorganization of alpha-hemoglobin. Gell DA, Feng L, Zhou S, Jeffrey PD, Bendak K, Gow A, Weiss MJ, Shi Y, Mackay JP. J Biol Chem 284 29462-29469 (2009)
  12. Linking COVID-19 and Heme-Driven Pathophysiologies: A Combined Computational-Experimental Approach. Hopp MT, Domingo-Fernández D, Gadiya Y, Detzel MS, Graf R, Schmalohr BF, Kodamullil AT, Imhof D, Hofmann-Apitius M. Biomolecules 11 644 (2021)
  13. Prediction of Protein Complex Structure Using Surface-Induced Dissociation and Cryo-Electron Microscopy. Seffernick JT, Canfield SM, Harvey SR, Wysocki VH, Lindert S. Anal Chem 93 7596-7605 (2021)
  14. Study of Functional and Allosteric Sites in Protein Superfamilies. Suplatov D, Švedas V. Acta Naturae 7 34-45 (2015)
  15. Protein Interaction Z Score Assessment (PIZSA): an empirical scoring scheme for evaluation of protein-protein interactions. Roy AA, Dhawanjewar AS, Sharma P, Singh G, Madhusudhan MS. Nucleic Acids Res 47 W331-W337 (2019)
  16. A 45-ns molecular dynamics simulation of hemoglobin in water by vectorizing and parallelizing COSMOS90 on the earth simulator: dynamics of tertiary and quaternary structures. Saito M, Okazaki I. J Comput Chem 28 1129-1136 (2007)
  17. Expanding the Scope of Cross-Link Identifications by Incorporating Collisional Activated Dissociation and Ultraviolet Photodissociation Methods. Cammarata MB, Macias LA, Rosenberg J, Bolufer A, Brodbelt JS. Anal Chem 90 6385-6389 (2018)
  18. Molecular interaction of silicon quantum dot micelles with plasma proteins: hemoglobin and thrombin. Chinnathambi S, Karthikeyan S, Hanagata N, Shirahata N. RSC Adv 9 14928-14936 (2019)
  19. Potential roles of inorganic phosphate on the progression of initially bound glucopyranose toward the nonenzymatic glycation of human hemoglobin: mechanistic diversity and impacts on site selectivity. Smith BA, Mottishaw CR, Hendricks AJ, Mitchell J, Becker S, Ropski PS, Park B, Finkbeiner-Caufield M, Garay-Nontol B, Holman RW, Rodnick KJ. Cogent Biol 4 1425196 (2018)
  20. GRPY: An Accurate Bead Method for Calculation of Hydrodynamic Properties of Rigid Biomacromolecules. Zuk PJ, Cichocki B, Szymczak P. Biophys J 115 782-800 (2018)
  21. Multiscale Modeling of Bio-Nano Interactions of Zero-Valent Silver Nanoparticles. Subbotina J, Lobaskin V. J Phys Chem B 126 1301-1314 (2022)
  22. A Novel In Silico Benchmarked Pipeline Capable of Complete Protein Analysis: A Possible Tool for Potential Drug Discovery. Perera DDBD, Perera KML, Peiris DC. Biology (Basel) 10 1113 (2021)
  23. Mapping blood biochemistry by Raman spectroscopy at the cellular level. Volkov VV, McMaster J, Aizenberg J, Perry CC. Chem Sci 13 133-140 (2021)
  24. ProtNN: fast and accurate protein 3D-structure classification in structural and topological space. Dhifli W, Diallo AB. BioData Min 9 30 (2016)
  25. Simulation of Energy-Resolved Mass Spectrometry Distributions from Surface-Induced Dissociation. Seffernick JT, Turzo SBA, Harvey SR, Kim Y, Somogyi Á, Marciano S, Wysocki VH, Lindert S. Anal Chem 94 10506-10514 (2022)
  26. Peroxidase activity and involvement in the oxidative stress response of roseobacter denitrificans truncated hemoglobin. Wang Y, Barbeau X, Bilimoria A, Lagüe P, Couture M, Tang JK. PLoS One 10 e0117768 (2015)
  27. Quaternary Structure Transitions of Human Hemoglobin: An Atomic-Level View of the Functional Intermediate States. Balasco N, Alba J, D'Abramo M, Vitagliano L. J Chem Inf Model 61 3988-3999 (2021)
  28. Structural Basis of Sequential and Concerted Cooperativity. Morea V, Angelucci F, Tame JRH, Di Cera E, Bellelli A. Biomolecules 12 1651 (2022)
  29. Antichaperone activity and heme degradation effect of methyl tert-butyl ether (MTBE) on normal and diabetic hemoglobins. Najdegerami IH, Maghami P, Sheikh-Hasani V, Hosseinzadeh G, Sheibani N, Moosavi-Movahedi AA. J Mol Recognit 30 (2017)
  30. Insights into the Progression of Labile Hb A1c to Stable Hb A1c via a Mechanistic Assessment of 2,3-Bisphosphoglycerate Facilitation of the Slow Nonenzymatic Glycation Process. Mottishaw CR, Becker S, Smith B, Titus G, Holman RW, Rodnick KJ. Hemoglobin 43 42-49 (2019)
  31. New Evidence for the Diversity of Mechanisms and Protonated Schiff Bases Formed in the Non-Enzymatic Covalent Protein Modification (NECPM) of HbA by the Hydrate and Aldehydic Forms of Acetaldehyde and Glyceraldehyde. Lewis J, Smith BA, Oakes H, Holman RW, Rodnick KJ. Cogent Biol 5 1584955 (2019)
  32. Resveratrol, a New Allosteric Effector of Hemoglobin, Enhances Oxygen Supply Efficiency and Improves Adaption to Acute Severe Hypoxia. Chu Z, Li W, You G, Chen Y, Qin D, Shu P, Wang Y, Wang Y, Zhao L, Zhou H. Molecules 28 2050 (2023)
  33. Selective and sensitive fluorescent staining of serum albumin in protein gel electrophoresis via sequence-defined oligo-dithiocarbamate. Jose A, Porel M. RSC Adv 13 35791-35798 (2023)
  34. The C-terminal 32-mer fragment of hemoglobin alpha is an amyloidogenic peptide with antimicrobial properties. Olari LR, Bauer R, Gil Miró M, Vogel V, Cortez Rayas L, Groß R, Gilg A, Klevesath R, Rodríguez Alfonso AA, Kaygisiz K, Rupp U, Pant P, Mieres-Pérez J, Steppe L, Schäffer R, Rauch-Wirth L, Conzelmann C, Müller JA, Zech F, Gerbl F, Bleher J, Preising N, Ständker L, Wiese S, Thal DR, Haupt C, Jonker HRA, Wagner M, Sanchez-Garcia E, Weil T, Stenger S, Fändrich M, von Einem J, Read C, Walther P, Kirchhoff F, Spellerberg B, Münch J. Cell Mol Life Sci 80 151 (2023)


Reviews citing this publication (12)

  1. The stereochemical mechanism of the cooperative effects in hemoglobin revisited. Perutz MF, Wilkinson AJ, Paoli M, Dodson GG. Annu Rev Biophys Biomol Struct 27 1-34 (1998)
  2. How useful is ion mobility mass spectrometry for structural biology? The relationship between protein crystal structures and their collision cross sections in the gas phase. Jurneczko E, Barran PE. Analyst 136 20-28 (2011)
  3. Cytochrome b559 of photosystem II. Stewart DH, Brudvig GW. Biochim Biophys Acta 1367 63-87 (1998)
  4. Hemoglobin variants: biochemical properties and clinical correlates. Thom CS, Dickson CF, Gell DA, Weiss MJ. Cold Spring Harb Perspect Med 3 a011858 (2013)
  5. Spectroscopic features of cytochrome P450 reaction intermediates. Luthra A, Denisov IG, Sligar SG. Arch Biochem Biophys 507 26-35 (2011)
  6. Hemoglobin: Structure, Function and Allostery. Ahmed MH, Ghatge MS, Safo MK. Subcell Biochem 94 345-382 (2020)
  7. Synthetic Fe/Cu Complexes: Toward Understanding Heme-Copper Oxidase Structure and Function. Adam SM, Wijeratne GB, Rogler PJ, Diaz DE, Quist DA, Liu JJ, Karlin KD. Chem Rev 118 10840-11022 (2018)
  8. Artificial allosteric receptors. Kremer C, Lützen A. Chemistry 19 6162-6196 (2013)
  9. Cooperativity and allostery in haemoglobin function. Ciaccio C, Coletta A, De Sanctis G, Marini S, Coletta M. IUBMB Life 60 112-123 (2008)
  10. From protein structure to function via single crystal optical spectroscopy. Ronda L, Bruno S, Bettati S, Storici P, Mozzarelli A. Front Mol Biosci 2 12 (2015)
  11. Carbon Dioxide and the Carbamate Post-Translational Modification. Blake LI, Cann MJ. Front Mol Biosci 9 825706 (2022)
  12. Crystallographic evidence for dioxygen interactions with iron proteins. Carrondo MA, Bento I, Matias PM, Lindley PF. J Biol Inorg Chem 12 429-442 (2007)

Articles citing this publication (56)

  1. 1.25 A resolution crystal structures of human haemoglobin in the oxy, deoxy and carbonmonoxy forms. Park SY, Yokoyama T, Shibayama N, Shiro Y, Tame JR. J Mol Biol 360 690-701 (2006)
  2. Residues crucial for maintaining short paths in network communication mediate signaling in proteins. del Sol A, Fujihashi H, Amoros D, Nussinov R. Mol Syst Biol 2 2006.0019 (2006)
  3. Application of the PM6 method to modeling proteins. Stewart JJ. J Mol Model 15 765-805 (2009)
  4. Modular architecture of protein structures and allosteric communications: potential implications for signaling proteins and regulatory linkages. Del Sol A, Araúzo-Bravo MJ, Amoros D, Nussinov R. Genome Biol 8 R92 (2007)
  5. Heme cytotoxicity and the pathogenesis of immune-mediated inflammatory diseases. Larsen R, Gouveia Z, Soares MP, Gozzelino R. Front Pharmacol 3 77 (2012)
  6. High and low oxygen affinity conformations of T state hemoglobin. Bruno S, Bonaccio M, Bettati S, Rivetti C, Viappiani C, Abbruzzetti S, Mozzarelli A. Protein Sci 10 2401-2407 (2001)
  7. New insights into the allosteric mechanism of human hemoglobin from molecular dynamics simulations. Mouawad L, Perahia D, Robert CH, Guilbert C. Biophys J 82 3224-3245 (2002)
  8. Novel mechanisms of pH sensitivity in tuna hemoglobin: a structural explanation of the root effect. Yokoyama T, Chong KT, Miyazaki G, Morimoto H, Shih DT, Unzai S, Tame JR, Park SY. J Biol Chem 279 28632-28640 (2004)
  9. The crystal structure of bar-headed goose hemoglobin in deoxy form: the allosteric mechanism of a hemoglobin species with high oxygen affinity. Liang Y, Hua Z, Liang X, Xu Q, Lu G. J Mol Biol 313 123-137 (2001)
  10. A tractable genotype-phenotype map modelling the self-assembly of protein quaternary structure. Greenbury SF, Johnston IG, Louis AA, Ahnert SE. J R Soc Interface 11 20140249 (2014)
  11. R-state haemoglobin with low oxygen affinity: crystal structures of deoxy human and carbonmonoxy horse haemoglobin bound to the effector molecule L35. Yokoyama T, Neya S, Tsuneshige A, Yonetani T, Park SY, Tame JR. J Mol Biol 356 790-801 (2006)
  12. A test of the role of the proximal histidines in the Perutz model for cooperativity in haemoglobin. Barrick D, Ho NT, Simplaceanu V, Dahlquist FW, Ho C. Nat Struct Biol 4 78-83 (1997)
  13. Allosteric effectors do not alter the oxygen affinity of hemoglobin crystals. Mozzarelli A, Rivetti C, Rossi GL, Eaton WA, Henry ER. Protein Sci 6 484-489 (1997)
  14. Allosteric mechanism of haemoglobin: rupture of salt-bridges raises the oxygen affinity of the T-structure. Bettati S, Mozzarelli A, Perutz MF. J Mol Biol 281 581-585 (1998)
  15. Alkylation of human hemoglobin A0 by the antimalarial drug artemisinin. Selmeczi K, Robert A, Claparols C, Meunier B. FEBS Lett 556 245-248 (2004)
  16. Experiments on Hemoglobin in Single Crystals and Silica Gels Distinguish among Allosteric Models. Henry ER, Mozzarelli A, Viappiani C, Abbruzzetti S, Bettati S, Ronda L, Bruno S, Eaton WA. Biophys J 109 1264-1272 (2015)
  17. Rapid reprogramming of haemoglobin structure-function exposes multiple dual-antimicrobial potencies. Du R, Ho B, Ding JL. EMBO J 29 632-642 (2010)
  18. The X-ray structure determination of bovine carbonmonoxy hemoglobin at 2.1 A resoultion and its relationship to the quaternary structures of other hemoglobin crystal froms. Safo MK, Abraham DJ. Protein Sci 10 1091-1099 (2001)
  19. Differential control of heme reactivity in alpha and beta subunits of hemoglobin: a combined Raman spectroscopic and computational study. Jones EM, Monza E, Balakrishnan G, Blouin GC, Mak PJ, Zhu Q, Kincaid JR, Guallar V, Spiro TG. J Am Chem Soc 136 10325-10339 (2014)
  20. High resolution crystal structure of deoxy hemoglobin from Trematomus bernacchii at different pH values: the role of histidine residues in modulating the strength of the root effect. Mazzarella L, Vergara A, Vitagliano L, Merlino A, Bonomi G, Scala S, Verde C, di Prisco G. Proteins 65 490-498 (2006)
  21. Magnesium(II) and zinc(II)-protoporphyrin IX's stabilize the lowest oxygen affinity state of human hemoglobin even more strongly than deoxyheme. Miyazaki G, Morimoto H, Yun KM, Park SY, Nakagawa A, Minagawa H, Shibayama N. J Mol Biol 292 1121-1136 (1999)
  22. What is the true structure of liganded haemoglobin? Tame JR. Trends Biochem Sci 24 372-377 (1999)
  23. A combinatorial approach to detect coevolved amino acid networks in protein families of variable divergence. Baussand J, Carbone A. PLoS Comput Biol 5 e1000488 (2009)
  24. WAXS studies of the structural diversity of hemoglobin in solution. Makowski L, Bardhan J, Gore D, Lal J, Mandava S, Park S, Rodi DJ, Ho NT, Ho C, Fischetti RF. J Mol Biol 408 909-921 (2011)
  25. Energetic components of the allosteric machinery in hemoglobin measured by hydrogen exchange. Englander JJ, Louie G, McKinnie RE, Englander SW. J Mol Biol 284 1695-1706 (1998)
  26. Tension in haemoglobin revealed by Fe-His(F8) bond rupture in the fully liganded T-state. Paoli M, Dodson G, Liddington RC, Wilkinson AJ. J Mol Biol 271 161-167 (1997)
  27. Coarse-grained and all-atom modeling of structural states and transitions in hemoglobin. Tekpinar M, Zheng W. Proteins 81 240-252 (2013)
  28. New insight into the mechanism of mitochondrial cytochrome c function. Chertkova RV, Brazhe NA, Bryantseva TV, Nekrasov AN, Dolgikh DA, Yusipovich AI, Sosnovtseva O, Maksimov GV, Rubin AB, Kirpichnikov MP. PLoS One 12 e0178280 (2017)
  29. NO binding to naphthalene dioxygenase. Karlsson A, Parales JV, Parales RE, Gibson DT, Eklund H, Ramaswamy S. J Biol Inorg Chem 10 483-489 (2005)
  30. Circular dichroism spectroscopy of tertiary and quaternary conformations of human hemoglobin entrapped in wet silica gels. Ronda L, Bruno S, Viappiani C, Abbruzzetti S, Mozzarelli A, Lowe KC, Bettati S. Protein Sci 15 1961-1967 (2006)
  31. Signal transmission between subunits in the hemoglobin T-state. Englander JJ, Rumbley JN, Englander SW. J Mol Biol 284 1707-1716 (1998)
  32. Flow Alignment of Extracellular Vesicles: Structure and Orientation of Membrane-Associated Bio-macromolecules Studied with Polarized Light. Szigyártó IC, Deák R, Mihály J, Rocha S, Zsila F, Varga Z, Beke-Somfai T. Chembiochem 19 545-551 (2018)
  33. Antibody-like Biorecognition Sites for Proteins from Surface Imprinting on Nanoparticles. Bhakta S, Seraji MS, Suib SL, Rusling JF. ACS Appl Mater Interfaces 7 28197-28206 (2015)
  34. Heterotropic effectors exert more significant strain on monoligated than on unligated hemoglobin. Coletta M, Angeletti M, Ascone I, Boumis G, Castellano AC, Dell'Ariccia M, Della Longa S, De Sanctis G, Priori AM, Santucci R, Feis A, Amiconi G. Biophys J 76 1532-1536 (1999)
  35. Catalytic competence of O-acetylserine sulfhydrylase in the crystal probed by polarized absorption microspectrophotometry. Mozzarelli A, Bettati S, Pucci AM, Burkhard P, Cook PF. J Mol Biol 283 135-146 (1998)
  36. Oxygen binding by alpha(Fe2+)2beta(Ni2+)2 hemoglobin crystals. Bruno S, Bettati S, Manfredini M, Mozzarelli A, Bolognesi M, Deriu D, Rosano C, Tsuneshige A, Yonetani T, Henry ER. Protein Sci 9 683-692 (2000)
  37. Reaction trajectory revealed by a joint analysis of protein data bank. Ren Z. PLoS One 8 e77141 (2013)
  38. A Modular Programmable Inorganic Cluster Discovery Robot for the Discovery and Synthesis of Polyoxometalates. Salley DS, Keenan GA, Long DL, Bell NL, Cronin L. ACS Cent Sci 6 1587-1593 (2020)
  39. Crystal structure of Lysbeta(1)82-Lysbeta(2)82 crosslinked hemoglobin: a possible allosteric intermediate. Fernandez EJ, Abad-Zapatero C, Olsen KW. J Mol Biol 296 1245-1256 (2000)
  40. Correlation of protein functional properties in the crystal and in solution: the case study of T-state hemoglobin. Noble RW, Kwiatkowski LD, Hui HL, Bruno S, Bettati S, Mozzarelli A. Protein Sci 11 1845-1849 (2002)
  41. Serum proteomic profiling in granumomatosis with polyangiitis using two-dimensional gel electrophoresis along with matrix assisted laser desorption ionization time of flight mass spectrometry. Rani L, Minz RW, Arora A, Kannan M, Sharma A, Anand S, Gupta D, Panda NK, Sakhuja VK. Int J Rheum Dis 17 910-919 (2014)
  42. Assessing local structural perturbations in proteins. Lema MA, Echave J. BMC Bioinformatics 6 226 (2005)
  43. Assessment of Cysteine Reactivity of Human Hemoglobin at Its Residue Level: A Mass Spectrometry-Based Approach. Mitra A, Muralidharan M, Srivastava D, Das R, Bhat V, Mandal AK. Hemoglobin 41 300-305 (2017)
  44. Photo-dissociation quantum yields of mammalian oxyhemoglobin investigated by a nanosecond laser technique. Yang NL, Zhang SY, Kuo PK, Qu M, Fang JW, Li JH, Hua ZC. Biochem Biophys Res Commun 353 953-959 (2007)
  45. Thalassemia major phenotype caused by HB Zürich-Albisrieden [α2 59(E8) Gly > Arg (HBA2:C.178G > C)] in a Brazilian child. Pedroso GA, Kimura EM, Santos MNN, Albuquerque DM, Malimpensa D, Jorge SE, Verissimo MPA, Costa FF, Sonati MF. Pediatr Blood Cancer 65 e27413 (2018)
  46. Thermal-induced force release in oxyhemoglobin. Gevorkian SG, Allahverdyan AE, Gevorgyan DS, Hu CK. Sci Rep 5 13064 (2015)
  47. pH-dependent structural changes in haemoglobin component V from the midge larva Propsilocerus akamusi (Orthocladiinae, Diptera). Kuwada T, Hasegawa T, Takagi T, Sato I, Shishikura F. Acta Crystallogr D Biol Crystallogr 66 258-267 (2010)
  48. Analysis of the Quaternary Structure of Hemoglobin Beckman Variant and Molecular Interpretation of Its Functional Abnormality: A Mass-Spectrometry-Based Approach. Muralidharan M, Das R, Bhat V, Mandal AK. Chembiochem 19 633-640 (2018)
  49. Biointeraction of Erythrocyte Ghost Membranes with Gold Nanoparticles Fluorescents. Gómez Flores V, Martínez-Martínez A, Roacho Pérez JA, Acosta Bezada J, Aguirre-Tostado FS, García Casillas PE. Materials (Basel) 14 6390 (2021)
  50. Computational strategy for visualizing structures and teaching biochemistry. Abreu PA, Carvalho KL, Rabelo VW, Castro HC. Biochem Mol Biol Educ 47 76-84 (2019)
  51. Movements at the hemoglobin A-hemes and their role in ligand binding, analyzed by X-ray crystallography. Dodson E, Dodson G. Biopolymers 91 1056-1063 (2009)
  52. Photolyses of mammalian oxy-hemoglobin studied by nanosecond photoacoustic calorimetry. Yang NL, Zhang SY, Qu M, Li JH, Hua ZC. Arch Biochem Biophys 466 78-84 (2007)
  53. Self-Assembly of Covalently Linked Porphyrin Dimers at the Solid-Liquid Interface. Habets T, Lensen D, Speller S, Elemans JAAW. Molecules 24 E3018 (2019)
  54. Influence of mutations at the proximal histidine position on the Fe-O2 bond in hemoglobin from density functional theory. Todde G, Hovmöller S, Laaksonen A. J Chem Phys 144 095101 (2016)
  55. Mixed, nonclassical behavior in a classic allosteric protein. Sapienza PJ, Bonin JP, Jinasena HPD, Li K, Dieckhaus H, Popov KI, Aubé J, Lee AL. Proc Natl Acad Sci U S A 120 e2308338120 (2023)
  56. Molecular modeling and small angle X-ray scattering studies of Hoplosternum littorale cathodic haemoglobin. Peres P, Lombardi FR, Dos Santos GC, Olivieri JR, Canduri F, Bonilla-Rodriguez GO, de Azevedo WF. Biochem Biophys Res Commun 325 487-493 (2004)