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Biomedical subjects

W E Royer

Publications and source records attributed to W E Royer.

At least 19 recordsLinked to original sources

Restricting the ligand-linked heme movement in Scapharca dimeric hemoglobin reveals tight coupling between distal and proximal contributions to cooperativity.

Cooperative ligand binding in the dimeric hemoglobin from the blood clam Scapharca inaequivalvis results primarily from tertiary, rather than quaternary, structural changes. Ligand binding is coupled with conformational changes of key residues, including Phe 97, which is extruded from the proximal heme pocket, and the heme group, which moves deeper into the heme pocket. We have tested the role of the heme movement in cooperative function by mutating Ile 114, at the base of the heme pocket. Replacement of this residue with a Met did not disturb the hemoglobin structure or significantly alter equilibrium ligand binding properties. In contrast, substitution with a Phe at position 114 inhibits the ligand-linked movement of the heme group, and substantially reduces oxygen affinity and cooperativity. As the extent of heme movement to the normal position of the ligated state is diminished, Phe 97 is inhibited from its movement into the interface upon ligand binding. These results indicate a tight coupling between these two key cooperative transitions and suggest that the heme movement may be an obligatory trigger for expulsion of Phe 97 from the heme pocket.

Amino Acid Sequence↗

Crystalline ligand transitions in lamprey hemoglobin. Structural evidence for the regulation of oxygen affinity.

The hemoglobins of the Sea Lamprey (Petromyzon marinus) exist in an equilibrium between low affinity oligomers, stabilized by proton binding, and higher affinity monomers, stabilized by oxygen binding. Recent crystallographic analysis revealed that dimerization is coupled with key changes at the ligand binding site with the distal histidine sterically restricting ligand binding in the deoxy dimer but with no significant structural rearrangements on the proximal side. These structural insights led to the hypothesis that oxygen affinity of lamprey hemoglobin is distally regulated. Here we present the 2.9-A crystal structure of deoxygenated lamprey hemoglobin in an orthorhombic crystal form along with the structure of these crystals exposed to carbon monoxide. The hexameric assemblage in this crystal form is very similar to those observed in the previous deoxy structure. Whereas the hydrogen bonding network and packing contacts formed in the dimeric interface of lamprey hemoglobin are largely unaffected by ligand binding, the binding of carbon monoxide induces the distal histidine to swing to positions that would preclude the formation of a stabilizing hydrogen bond with the bound ligand. These results suggest a dual role for the distal histidine and strongly support the hypothesis that ligand affinity in lamprey hemoglobin is distally regulated.

Animals↗

Cooperative hemoglobins: conserved fold, diverse quaternary assemblies and allosteric mechanisms.

Assembly of hemoglobin subunits into cooperative complexes produces a remarkable variety of architectures, ranging in oligomeric state from dimers to complexes containing 144 hemoglobin subunits. Diverse stereochemical mechanisms for modulating ligand affinity through intersubunit interactions have been revealed from studies of three distinct hemoglobin assemblages. This mechanistic diversity, which occurs between assemblies of subunits that have the same fold, provides insight into the range of regulatory strategies that are available to protein molecules.

Allosteric Site↗

Structural hierarchy in erythrocruorin, the giant respiratory assemblage of annelids.

Many annelids, including the earthworm Lumbricus terrestris, have giant cooperative respiratory proteins (molecular masses greater than 3.5 million Da) freely dissolved in the blood, rather than packaged in cells. These complexes, termed either erythrocruorins or hemoglobins, are assembled from many copies of both hemoglobin subunits and nonhemoglobin or "linker" subunits. In this paper, we present the crystal structure of Lumbricus erythrocruorin at 5.5-A resolution, which reveals a remarkable hierarchical organization of 144 oxygen-binding hemoglobin subunits and 36 nonhemoglobin linker subunits. The hemoglobin chains arrange in novel dodecameric substructures. Twelve trimeric linker complexes project triple-stranded helical coiled-coil "spokes" toward the center of the complex; interdigitation of these spokes appears crucial for stabilization. The resulting complex of linker chains forms a scaffold on which twelve hemoglobin dodecamers assemble. This structure specifies the unique, self-limited assemblage of a highly cooperative single molecule.

Animals↗

X-Ray crystal structure and molecular dynamics simulations of silver hake parvalbumin (Isoform B).

Parvalbumins constitute a class of calcium-binding proteins characterized by the presence of several helix-loop-helix (EF-hand) motifs. In a previous study (Revett SP, King G, Shabanowitz J, Hunt DF, Hartman KL, Laue TM, Nelson DJ, 1997, Protein Sci 7:2397-2408), we presented the sequence of the major parvalbumin isoform from the silver hake (Merluccius bilinearis) and presented spectroscopic and structural information on the excised "EF-hand" portion of the protein. In this study, the X-ray crystal structure of the silver hake major parvalbumin has been determined to high resolution, in the frozen state, using the molecular replacement method with the carp parvalbumin structure as a starting model. The crystals are orthorhombic, space group C2221, with a = 75.7 A, b = 80.7 A, and c = 42.1 A. Data were collected from a single crystal grown in 15% glycerol, which served as a cryoprotectant for flash freezing at -188 degrees C. The structure refined to a conventional R-value of 21% (free R 25%) for observed reflections in the range 8 to 1.65 A [1 > 2sigma(I)]. The refined model includes an acetylated amino terminus, 108 residues (characteristic of a beta parvalbumin lineage), 2 calcium ions, and 114 water molecules per protein molecule. The resulting structure was used in molecular dynamics (MD) simulations focused primarily on the dynamics of the ligands coordinating the Ca2+ ions in the CD and EF sites. MD simulations were performed on both the fully Ca2+ loaded protein and on a Ca2+ deficient variant, with Ca2+ only in the CD site. There was substantial agreement between the MD and X-ray results in addressing the issue of mobility of key residues in the calcium-binding sites, especially with regard to the side chain of Ser55 in the CD site and Asp92 in the EF site.

Animals↗

The 2.7 A crystal structure of deoxygenated hemoglobin from the sea lamprey (Petromyzon marinus): structural basis for a lowered oxygen affinity and Bohr effect.

BACKGROUND: The hemoglobins of the sea lamprey are unusual in that cooperativity and sensitivity to pH arise from an equilibrium between a high-affinity monomer and a low-affinity oligomer. Although the crystal structure of the monomeric cyanide derivative has previously been determined, the manner by which oligomerization acts to lower the oxygen affinity and confer a strong Bohr effect has, until now, been speculative. RESULTS: We have determined the crystal structure of deoxygenated lamprey hemoglobin V by molecular replacement to 2.7 A resolution, in a crystal form with twelve protomers in the asymmetric unit. The subunits are arranged as six essentially identical dimers, with a novel subunit interface formed by the E helices and the AB corner using the standard hemoglobin helical designations. In addition to nonpolar interactions, the interface includes a striking cluster of four glutamate residues. The proximity of the interface to ligand-binding sites implicates a direct effect on ligand affinity. CONCLUSIONS: Comparison of the deoxy structure with that of the cyanide derivative revealed conformational changes that appear to be linked to the functional behavior. Oligomerization is coupled with a movement of the first half of the E helix by up to 1.0 A towards the heme, resulting in steric interference of ligand binding to the deoxy structure. The Bohr effect seems to result from proton uptake by glutamate residues as they are buried in the interface. Unlike human and mollusc hemoglobins, in which modulation of function is due to primarily proximal effects, regulation of oxygen affinity in lamprey hemoglobin V seems to depend on changes at the distal (ligand-binding) side of the heme group.

Animals↗

Mutational destabilization of the critical interface water cluster in Scapharca dimeric hemoglobin: structural basis for altered allosteric activity.

A cluster of interface ordered water molecules has been proposed to act as a key mediator of intersubunit communication in the homodimeric hemoglobin of Scapharca inaequivalvis. Mutations of Thr72 to Val and Ile, which lack the hydroxyl group to hydrogen bond the deoxy interface water molecules, result in sharply altered functional properties. We have determined the high resolution (1.6-1. 8 A) crystal structures of these two mutants in both the deoxygenated and CO-liganded states. These structures show minimal protein structural changes relative to the same native derivatives, despite greater than 40-fold increases in oxygen affinity. In the deoxy state of both mutants two water molecules at the periphery of the water cluster are lost, and the remaining cluster water molecules are destabilized. The CO-liganded structures show key differences between the two mutants including a more optimal interface packing involving Ile72 that acts to stabilize its high affinity (R) state. This additional stabilization allows rationalization of its lowered cooperativity within the context of a two-state model. These studies support a key role of ordered water in cooperative functioning and illustrate how subtle structural alterations can result in significantly altered functional properties in an allosteric molecule.

Allosteric Regulation↗

Crystal structure of deoxy-human hemoglobin beta6 Glu --> Trp. Implications for the structure and formation of the sickle cell fiber.

An atomic-level understanding of the interactions between hemoglobin molecules that contribute to the formation of pathological fibers in sickle cell disease remains elusive. By exploring crystal structures of mutant hemoglobins with altered polymerization properties, insight can be gained into sickle cell hemoglobin (HbS) polymerization. We present here the 2.0-A resolution deoxy crystal structure of human hemoglobin mutated to tryptophan at the beta6 position, the site of the glutamate --> valine mutation in HbS. Unlike leucine and isoleucine, which promote polymerization relative to HbS, tryptophan inhibits polymerization. Our results provide explanations for the altered polymerization properties and reveal a fundamentally different double strand that may provide a model for interactions within a fiber and/or interactions leading to heterogeneous nucleation.

Amino Acid Substitution↗

The high resolution crystal structure of deoxyhemoglobin S.

We have refined the crystal structure of deoxyhemoglobin S (beta Glu6-->Val) at 2.05 A resolution to an R-factor of 16.5% (free R=21. 5%) using crystals isomorphous to those originally grown by Wishner and Love. A predominant feature of this crystal form is a double strand of hemoglobin tetramers that has been shown by a variety of techniques to be the fundamental building block of the intracellular sickle cell fiber. The double strand is stabilized by lateral contacts involving the mutant valine interacting with a pocket between the E and F helices on another tetramer. The new structure reveals some marked differences from the previously refined 3.0 A resolution structure, including several residues in the lateral contact which have shifted by as much as 3.5 A. The lateral contact includes, in addition to the hydrophobic interactions involving the mutant valine, hydrophilic interactions and bridging water molecules at the periphery of the contact. This structure provides further insights into hemoglobin polymerization and may be useful for the structure-based design of therapeutic agents to treat sickle cell disease.

Anemia, Sickle Cell↗

Mutation of residue Phe97 to Leu disrupts the central allosteric pathway in Scapharca dimeric hemoglobin.

Residue Phe97, which is thought to play a central role in the cooperative functioning of Scapharca dimeric hemoglobin, has been mutated to leucine to test its proposed role in mediating cooperative oxygen binding. This results in an 8-fold increase in oxygen affinity and a marked decrease in cooperativity. Kinetic measurements of ligand binding to the Leu97 mutant suggest an altered unliganded (deoxy) state, which has been confirmed by high resolution crystal structures in the unliganded and carbon monoxide-liganded states. Analysis of the structures at allosteric end points reveals them to be remarkably similar to the corresponding wild-type structures, with differences confined to the disposition of residue 97 side chain, F-helix geometry, and the interface water structure. Increased oxygen affinity results from the absence of the Phe97 side chain, whose tight packing in the heme pocket of the deoxy state normally restricts the heme from assuming a high affinity conformation. The absence of the Phe97 side chain is also associated with diminished cooperativity, since Leu97 packs in the heme pocket in both states. Residual cooperativity appears to be coupled with observed structural transitions and suggests that parallel pathways for communication exist in Scapharca dimeric hemoglobin.

Allosteric Regulation↗

Ligand linked assembly of Scapharca dimeric hemoglobin.

The assembly of Scapharca dimeric hemoglobin as a function of ligation has been explored by analytical gel chromatography, sedimentation equilibrium, and oxygen binding experiments to test the proposal that its cooperativity is based on quaternary enhancement. This hypothesis predicts that the liganded form would be assembled more tightly into a dimer than the unliganded form and that dissociation would lead to lower oxygen affinity. Our experiments demonstrate that although the dimeric interface is quite tight in this hemoglobin, dissociation can be clearly detected in the liganded states with monomer to dimer association constants in the range of 10(8) M-1 for the CO-liganded state and lower association constants measured in the oxygenated state. In contrast, the deoxy dimer shows no detectable dissociation by analytical ultracentrifugation. Thus, the more highly hydrated deoxy interface of this dimer is also the more tightly assembled. Equilibrium oxygen binding experiments reveal an increase in oxygen affinity and decrease in cooperativity as the concentration is lowered (in the muM range). These experiments unambiguously refute the hypothesis of quaternary enhancement and indicate that, as in the case of human hemoglobin and other allosteric proteins, quaternary constraint underlies cooperativity in Scapharca dimeric hemoglobin.

Animals↗

Ordered water molecules as key allosteric mediators in a cooperative dimeric hemoglobin.

One of the most remarkable structural aspects of Scapharca dimeric hemoglobin is the disruption of a very well-ordered water cluster at the subunit interface upon ligand binding. We have explored the role of these crystallographically observed water molecules by site-directed mutagenesis and osmotic stress techniques. The isosteric mutation of Thr-72-->Val in the interface increases oxygen affinity more than 40-fold with a surprising enhancement of cooperativity. The only significant structural effect of this mutation is to destabilize two ordered water molecules in the deoxy interface. Wild-type Scapharca hemoglobin is strongly sensitive to osmotic conditions. Upon addition of glycerol, striking changes in Raman spectrum of the deoxy form are observed that indicate a transition toward the liganded form. Increased osmotic pressure, which lowers the oxygen affinity in human hemoglobin, raises the oxygen affinity of Scapharca hemoglobin regardless of whether the solute is glycerol, glucose, or sucrose. Analysis of these results provides an estimate of six water molecules lost upon oxygen binding to the dimer, in good agreement with eight predicted from crystal structures. These experiments suggest that the observed cluster of interfacial water molecules plays a crucial role in communication between subunits.

Allosteric Regulation↗

The 2.0 A crystal structure of Scapharca tetrameric hemoglobin: cooperative dimers within an allosteric tetramer.

The crystal structure of the allosteric tetrameric hemoglobin from Scapharca inaequivalvis (HbII) has been determined in the carbonmonoxy liganded state using a combination of anomalous scattering and molecular replacement. The molecular model has been refined at 2.0 A resolution to a conventional R-factor of 0.173 and a free R-factor of 0.244. The tetramer is formed from two identical heterodimers. Each heterodimer is assembled with intersubunit contacts involving the E and F helices and heme groups in a manner that is very similar to that of the cooperative Scapharca homodimeric hemoglobin. In addition, the ordered water structure observed in these dimeric interfaces is quite similar. These structural similarities strongly suggest that the dimers within the Scapharca tetramer are cooperative. Subunits assemble into a tetramer in a distinctly non-tetrahedral arrangement, with the pseudo 2-fold axes of the heterodimer oriented at an angle of 74.5 degrees relative to the molecular 2-fold. This arrangement requires that two subunit types have distinct locations and contacts, despite the very similar tertiary structures. HbII polymerizes to higher-order assemblages in a ligand, proton and anion dependent fashion. The lattice contacts in the HbII-CO crystal suggest possible modes for this association.

Allosteric Site↗

Bacterial expression of Scapharca dimeric hemoglobin: a simple model system for investigating protein cooperatively.

Recombinant Scapharca homodimeric hemoglobin has been expressed at high levels from a synthetic gene in Escherichia coli. Addition of the heme precursor delta-aminolevulinic acid to the expression culture results in a considerable increase in the yield of soluble hemoglobin. The recombinant hemoglobin exhibits cooperative oxygen binding properties indistinguishable from native protein. Crystals of the recombinant protein, like those of native hemoglobin, diffract to high resolution which will allow functional studies of site-directed mutants to be correlated with detailed structural analyses.

Amino Acid Sequence↗

Crystal structure of oxygenated Scapharca dimeric hemoglobin at 1.7-A resolution.

The crystal structure of the cooperative dimeric hemoglobin from the blood clam Scapharca inaequivalvis has been determined in the oxygenated state and refined to an R-factor of 0.157 at 1.7-A resolution. The structure is very similar to the carbon monoxide-liganded form with subtle differences in ligand binding geometry. Oxygen binds to the heme iron in a bent conformation with Fe-O-O angles of 135 degrees and 150 degrees for the two subunits. These observed angles are lower than the equivalent angles in the carbon monoxide-liganded form and intermediate between the angles observed in structures of oxygenated sperm whale myoglobin and oxygenated human hemoglobin. This third high resolution structure of Scapharca dimeric hemoglobin permits a detailed analysis of the water structure in the highly hydrated interface between subunits.

Animals↗

High-resolution crystallographic analysis of a co-operative dimeric hemoglobin.

High-resolution crystal structures of the co-operative dimeric hemoglobin from the blood clam Scapharca inaequivalvis have been determined in the unliganded (deoxy) and carbon monoxide (CO) liganded states. The deoxy structure has been refined at 1.6 A resolution to an R-factor of 0.158 and the CO structure has been refined at 1.4 A resolution to an R-factor of 0.159. These structures reveal details of the structural transitions involved in co-operative ligand binding that involve only a minor rotation of subunits but very striking tertiary changes at the interface. A small number of residues in the F-helix appear to mediate co-operativity in this simple hemoglobin. The oxygen affinity of each subunit appears to be largely dictated by the disposition of phenylalanine 97, whose side-chain packs in the heme pocket in the deoxy state but is extruded towards the interface in the CO-liganded structure. Direct involvement of the ligand-binding heme group is a novel feature of the subunit interface and appears important for intersubunit communication. Ligation alters the conformation of the heme propionate groups along with two interacting residues from the symmetry-related subunit. These two residues, lysine 96 and asparagine 100, link the heme of one subunit with the F-helix of the second subunit in such a way as to influence the ligand affinity of that subunit. The interface is highly hydrated by well-ordered water molecules that are likely to be important in the stabilization of the two structures.

Allosteric Regulation↗

Quantification of tertiary structural conservation despite primary sequence drift in the globin fold.

The globin family of protein structures was the first for which it was recognized that tertiary structure can be highly conserved even when primary sequences have diverged to a virtually undetectable level of similarity. This principle of structural inertia in molecular evolution is now evident for many other protein families. We have performed a systematic comparison of the sequences and structures of 6 representative hemoglobin subunits as diverse in origin as plants, clams, and humans. Our analysis is based on a 97-residue helical core in common to all 6 structures. Amino acid sequence identities range from 12.4% to 42.3% in pairwise comparisons, and, despite these variations, the maximal RMS deviation in alpha-carbon positions is 3.02 A. Overall, sequence similarity and structural deviation are significantly anticorrelated, with a correlation coefficient of -0.71, but for a set of structures having under 20% pairwise identity, this anticorrelation falls to -0.38, which emphasizes the weak connection between a specific sequence and the tertiary fold. There is substantial variability in structure outside the helical core, and functional characteristics of these globins also differ appreciably. Nevertheless, despite variations in detail that the sequence dissimilarities and functional differences imply, the core structures of these globins remain remarkably preserved.

Amino Acid Sequence↗

Ligand binding and conformation change in the dimeric hemoglobin of the clam Scapharca inaequivalvis.

The reaction with carbon monoxide of the cooperative dimeric hemoglobin from Scapharca inaequivalvis has been examined by flash photolysis. In the nanosecond time range, geminate rebinding of 5% of dissociated CO occurs with a rate constant of 1.4 x 10(7) s-1. There is a change in absorbance of deoxyhemoglobin following photolysis at a rate of 1.2 x 10(6) s-1, consistent with a shift in the position of the Soret band to longer wavelengths. The amplitude of the change is proportional to the population of deoxydimer. In much of the Soret region this change is greater than the absorbance excursion associated with geminate recombination. There is at least one other slower change associated with the singly liganded species. Geminate rebinding of NO has components of 50, 8, and 0.035 ns-1, accounting for 75%, 25%, and less than 1% of the total reaction observed after a 35-ps photolysis flash. Simulation of diffusion of NO by molecular dynamics shows the ligands moving from the heme pocket to a subsidiary space between the edge of the heme and the surface of the protein.

Animals↗