Salt bridge (protein and supramolecular)

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Figure 1. Example of salt bridge between amino acids glutamic acid and lysine demonstrating electrostatic interaction and hydrogen bonding Next Revisit Glutamic Acid Lysine salt bridge.png
Figure 1. Example of salt bridge between amino acids glutamic acid and lysine demonstrating electrostatic interaction and hydrogen bonding

In chemistry, a salt bridge is a combination of two non-covalent interactions: hydrogen bonding and ionic bonding (Figure 1). Ion pairing is one of the most important noncovalent forces in chemistry, in biological systems, in different materials and in many applications such as ion pair chromatography. It is a most commonly observed contribution to the stability to the entropically unfavorable folded conformation of proteins. Although non-covalent interactions are known to be relatively weak interactions, small stabilizing interactions can add up to make an important contribution to the overall stability of a conformer. [1] Not only are salt bridges found in proteins, but they can also be found in supramolecular chemistry. The thermodynamics of each are explored through experimental procedures to access the free energy contribution of the salt bridge to the overall free energy of the state.

Contents

Salt bridges in chemical bonding

In water, formation of salt bridges or ion pairs is mostly driven by entropy, usually accompanied by unfavorable ΔH contributions on account of desolvation of the interacting ions upon association. [2] Hydrogen bonds contribute to the stability of ion pairs with e.g. protonated ammonium ions, and with anions is formed by deprotonation as in the case of carboxylate, phosphate etc; then the association constants depend on the pH. Entropic driving forces for ion pairing (in absence of significant H-bonding contributions) are also found in methanol as solvent. In nonpolar solvents contact ion pairs with very high association constants are formed,; [3] [4] in the gas phase the association energies of e.g. alkali halides reach up to 200 kJ/mol. [5] The Bjerrum or the Fuoss equation describe ion pair association as function of the ion charges zA and zB and the dielectric constant ε of the medium; a corresponding plot of the stability ΔG vs. zAzB shows for over 200 ion pairs the expected linear correlation for a large variety of ions. [6] Inorganic as well as organic ions display at moderate ionic strength I similar salt bridge association ΔG values around 5 to 6 kJ/mol for a 1:1 combination of anion and cation, almost independent of the nature (size, polarizability etc) of the ions. [7] [8] The ΔG values are additive and approximately a linear function of the charges, the interaction of e.g. a doubly charged phosphate anion with a single charged ammonium cation accounts for about 2x5 = 10 kJ/mol. The ΔG values depend on the ionic strength I of the solution, as described by the Debye–Hückel equation, at zero ionic strength one observes ΔG = 8 kJ/mol. The stabilities of the alkali-ion pairs as function of the anion charge z by can be described by a more detailed equation. [9]

Salt bridges found in proteins

Figure 2. Wild type (left) and mutated (right) form of lamin A (LMNA, PDB: 1IFR). Normally, arginine 527 (blue) forms salt bridge with glutamate 537 (magenta), but R527L mutation causes loss of the complementary negative charge and structure destabilization. At the phenotype level this manifests with overlapping mandibuloacral dysplasia and progeria syndrome. LMNA protein (1ifr) mutation R527L PMID 22549407 surface and cartoon.png
Figure 2. Wild type (left) and mutated (right) form of lamin A (LMNA, PDB: 1IFR). Normally, arginine 527 (blue) forms salt bridge with glutamate 537 (magenta), but R527L mutation causes loss of the complementary negative charge and structure destabilization. At the phenotype level this manifests with overlapping mandibuloacral dysplasia and progeria syndrome.

The salt bridge most often arises from the anionic carboxylate (RCOO−) of either aspartic acid or glutamic acid and the cationic ammonium (RNH3+) from lysine or the guanidinium (RNHC(NH2)2+) of arginine (Figure 2). [1] Although these are the most common, other residues with ionizable side chains such as histidine, tyrosine, and serine can also participate, depending on outside factors perturbing their pKa's. The distance between the residues participating in the salt bridge is also cited as being important. The distance required is less than 4 Å (400 pm). Amino acids greater than this distance apart do not qualify as forming a salt bridge. [11] Due to the numerous ionizable side chains of amino acids found throughout a protein, the pH at which a protein is placed is crucial to its stability.

Salt bridges found in protein - ligand complexes

Salt bridges also can form between a protein and small molecule ligands. Over 1100 unique protein-ligand complexes from the Protein Databank were found to form salt bridges with their protein targets, indicating that salt bridges are frequent in drug-protein interaction. [12] These contain structures from different enzyme classes, including hydrolase, transferases, kinases, reductase, oxidoreductase, lyases, and G protein-coupled receptors (GPCRs). Recent studies have shown that salt bridges play an important role in stabilizing protein-ligand complexes by acting as molecular clips that stabilize the protein's conformation and may boost inhibitor activity by hundreds of folds. [13] Hence incorporating salt bridges between ligands and their protein targets could be a valuable tool in rational drug design.

Methods for quantifying salt bridge stability in proteins

Figure 3. A salt bridge in T4 lysozyme between aspartic acid (Asp) at residue 70 and a histidine (His) at residue 31 T4 lysozyme.png
Figure 3. A salt bridge in T4 lysozyme between aspartic acid (Asp) at residue 70 and a histidine (His) at residue 31

The contribution of a salt bridge to the overall stability to the folded state of a protein can be assessed through thermodynamic data gathered from mutagenesis studies and nuclear magnetic resonance techniques. [14] Using a mutated pseudo-wild-type protein specifically mutated to prevent precipitation at high pH, the salt bridge’s contribution to the overall free energy of the folded protein state can be determined by performing a point-mutation, altering and, consequently, breaking the salt bridge. For example, a salt bridge was identified to exist in the T4 lysozyme between aspartic acid (Asp) at residue 70 and a histidine (His) at residue 31 (Figure 3). Site-directed mutagenesis with asparagine (Asn) (Figure 4) was done obtaining three new mutants: Asp70Asn His31 (Mutant 1), Asp70 His31Asn (Mutant 2), and Asp70Asn His31Asn (Double Mutant).

Figure 4. Mutagenesis of T4 lysozyme salt bridge between Asp 70 and His 31 Revisited Double Mutant Asp70His31.png
Figure 4. Mutagenesis of T4 lysozyme salt bridge between Asp 70 and His 31

Once the mutants have been established, two methods can be employed to calculate the free energy associated with a salt bridge. One method involves the observation of the melting temperature of the wild-type protein versus that of the three mutants. The denaturation can be monitored through a change in circular dichroism. A reduction in melting temperature indicates a reduction in stability. This is quantified through a method described by Becktel and Schellman where the free energy difference between the two is calculated through ΔTΔS. [15] There are some issues with this calculation and can only be used with very accurate data.[ citation needed ] In the T4 lysozyme example, ΔS of the pseudo-wild-type had previously been reported at pH 5.5 so the midpoint temperature difference of 11 °C at this pH multiplied by the reported ΔS of 360 cal/(mol·K) (1.5 kJ/(mol·K)) yields a free energy change of about −4 kcal/mol (−17 kJ/mol). This value corresponds to the amount of free energy contributed to the stability of the protein by the salt bridge.

Figure 5. Titration curve between the wild-type (blue) and the mutant (red) WildGraph.png
Figure 5. Titration curve between the wild-type (blue) and the mutant (red)

The second method utilizes nuclear magnetic resonance spectroscopy to calculate the free energy of the salt bridge. A titration is performed, while recording the chemical shift corresponding to the protons of the carbon adjacent to the carboxylate or ammonium group. The midpoint of the titration curve corresponds to the pKa, or the pH where the ratio of protonated: deprotonated molecules is 1:1. Continuing with the T4 lysozyme example, a titration curve is obtained through observation of a shift in the C2 proton of histidine 31 (Figure 5). Figure 5 shows the shift in the titration curve between the wild-type and the mutant in which Asp70 is Asn. The salt bridge formed is between the deprotonated Asp70 and protonated His31. This interaction causes the shift seen in His31’s pKa. In the unfolded wild-type protein, where the salt bridge is absent, His31 is reported to have a pKa of 6.8 in H2O buffers of moderate ionic strength. Figure 5 shows a pKa of the wild-type of 9.05. This difference in pKa is supported by the His31’s interaction with Asp70. To maintain the salt bridge, His31 will attempt to keep its proton as long as possible. When the salt bridge is disrupted, like in the mutant D70N, the pKa shifts back to a value of 6.9, much closer to that of His31 in the unfolded state.

The difference in pKa can be quantified to reflect the salt bridge’s contribution to free energy. Using Gibbs free energy: ΔG = −RT ln(Keq), where R is the universal gas constant, T is the temperature in kelvins, and Keq is the equilibrium constant of a reaction in equilibrium. The deprotonation of His31 is an acid equilibrium reaction with a special Keq known as the acid dissociation constant, Ka: His31-H+⇌ His31 + H+. The pKa is then related to Ka by the following: pKa = −log(Ka). Calculation of the free energy difference of the mutant and wild-type can now be done using the free energy equation, the definition of pKa, the observed pKa values, and the relationship between natural logarithms and logarithms. In the T4 lysozyme example, this approach yielded a calculated contribution of about 3 kcal/mol to the overall free energy. [14] A similar approach can be taken with the other participant in the salt bridge, such as Asp70 in the T4 lysozyme example, by monitoring its shift in pKa after mutation of His31.

A word of caution when choosing the appropriate experiment involves the location of the salt bridge within the protein. The environment plays a large role in the interaction. [16] At high ionic strengths, the salt bridge can be completely masked since an electrostatic interaction is involved. The His31-Asp70 salt bridge in T4 lysozyme was buried within the protein. Entropy plays a larger role in surface salt bridges where residues that normally have the ability to move are constricted by their electrostatic interaction and hydrogen bonding. This has been shown to decrease entropy enough to nearly erase the contribution of the interaction. [17] Surface salt bridges can be studied similarly to that of buried salt bridges, employing double mutant cycles and NMR titrations. [18] Although cases exist where buried salt bridges contribute to stability, like anything else, exceptions do exist and buried salt bridges can display a destabilizing effect. [11] Also, surface salt bridges, under certain conditions, can display a stabilizing effect. [16] [18] The stabilizing or destabilizing effect must be assessed on a case by case basis and few blanket statements are able to be made.

Supramolecular chemistry

Figure 6. The "egg shell" molecular capsule Chem540f09capcartoon.png
Figure 6. The "egg shell" molecular capsule
Figure 7. Interlacing salt bridges that connect the two halves of the molecular capsule Chem540, Egg Schell2.png
Figure 7. Interlacing salt bridges that connect the two halves of the molecular capsule

Supramolecular chemistry is a field concerned with non-covalent interactions between macromolecules. Salt bridges have been used by chemists within this field in both diverse and creative ways, including sensing of anions, the synthesis of molecular capsules and double helical polymers.

Anion complexation

Major contributions of supramolecular chemistry have been devoted to recognition and sensing of anions. [19] [20] [21] [22] [23] [24] Ion pairing is the most important driving force for anion complexation, but selectivity e.g. within the halide series has been achieved, mostly by hydrogen bonds contributions.

Molecular capsules

Molecular capsules are chemical scaffolds designed to capture and hold a guest molecule (see molecular encapsulation). Szumna and coworkers developed a novel molecular capsule with a chiral interior. [25] This capsule is made of two halves, like a plastic easter egg (Figure 6). Salt bridge interactions between the two halves cause them to self-assemble in solution (Figure 7). They are stable even when heated to 60 °C.

Double helical polymers

Yashima and coworkers have used salt bridges to construct several polymers that adopt a double helix conformation much like DNA. [26] In one example, they incorporated platinum to create a double helical metallopolymer. [27] Starting from their monomer and platinum(II) biphenyl (Figure 8), their metallopolymer self assembles through a series of ligand exchange reactions. The two halves of the monomer are anchored together through the salt bridge between the deprotonated carboxylate and the protonated nitrogens.

Figure 8. Self-assembly of a double helical metallopolymer Metallopolymermed.gif
Figure 8. Self-assembly of a double helical metallopolymer

Related Research Articles

<span class="mw-page-title-main">Ionic bonding</span> Chemical bonding involving attraction between ions

Ionic bonding is a type of chemical bonding that involves the electrostatic attraction between oppositely charged ions, or between two atoms with sharply different electronegativities, and is the primary interaction occurring in ionic compounds. It is one of the main types of bonding, along with covalent bonding and metallic bonding. Ions are atoms with an electrostatic charge. Atoms that gain electrons make negatively charged ions. Atoms that lose electrons make positively charged ions. This transfer of electrons is known as electrovalence in contrast to covalence. In the simplest case, the cation is a metal atom and the anion is a nonmetal atom, but these ions can be more complex, e.g. molecular ions like NH+
4 or SO2−
4. In simpler words, an ionic bond results from the transfer of electrons from a metal to a non-metal to obtain a full valence shell for both atoms.

An intermolecular force (IMF) is the force that mediates interaction between molecules, including the electromagnetic forces of attraction or repulsion which act between atoms and other types of neighbouring particles, e.g. atoms or ions. Intermolecular forces are weak relative to intramolecular forces – the forces which hold a molecule together. For example, the covalent bond, involving sharing electron pairs between atoms, is much stronger than the forces present between neighboring molecules. Both sets of forces are essential parts of force fields frequently used in molecular mechanics.

<span class="mw-page-title-main">Ligand</span> Ion or molecule that binds to a central metal atom to form a coordination complex

In coordination chemistry, a ligand is an ion or molecule with a functional group that binds to a central metal atom to form a coordination complex. The bonding with the metal generally involves formal donation of one or more of the ligand's electron pairs, often through Lewis bases. The nature of metal–ligand bonding can range from covalent to ionic. Furthermore, the metal–ligand bond order can range from one to three. Ligands are viewed as Lewis bases, although rare cases are known to involve Lewis acidic "ligands".

In chemistry, an acid dissociation constant is a quantitative measure of the strength of an acid in solution. It is the equilibrium constant for a chemical reaction

<span class="mw-page-title-main">Allosteric regulation</span> Regulation of enzyme activity

In biochemistry, allosteric regulation is the regulation of an enzyme by binding an effector molecule at a site other than the enzyme's active site.

<span class="mw-page-title-main">Ionic compound</span> Chemical compound involving ionic bonding

In chemistry, an ionic compound is a chemical compound composed of ions held together by electrostatic forces termed ionic bonding. The compound is neutral overall, but consists of positively charged ions called cations and negatively charged ions called anions. These can be simple ions such as the sodium (Na+) and chloride (Cl−) in sodium chloride, or polyatomic species such as the ammonium (NH+
4) and carbonate (CO2−
3) ions in ammonium carbonate. Individual ions within an ionic compound usually have multiple nearest neighbours, so are not considered to be part of molecules, but instead part of a continuous three-dimensional network. Ionic compounds usually form crystalline structures when solid.

Supramolecular chemistry refers to the branch of chemistry concerning chemical systems composed of a discrete number of molecules. The strength of the forces responsible for spatial organization of the system range from weak intermolecular forces, electrostatic charge, or hydrogen bonding to strong covalent bonding, provided that the electronic coupling strength remains small relative to the energy parameters of the component. While traditional chemistry concentrates on the covalent bond, supramolecular chemistry examines the weaker and reversible non-covalent interactions between molecules. These forces include hydrogen bonding, metal coordination, hydrophobic forces, van der Waals forces, pi–pi interactions and electrostatic effects.

<span class="mw-page-title-main">Molecular recognition</span> Type of non-covalent bonding

The term molecular recognition refers to the specific interaction between two or more molecules through noncovalent bonding such as hydrogen bonding, metal coordination, hydrophobic forces, van der Waals forces, π-π interactions, halogen bonding, or resonant interaction effects. In addition to these direct interactions, solvents can play a dominant indirect role in driving molecular recognition in solution. The host and guest involved in molecular recognition exhibit molecular complementarity. Exceptions are molecular containers, including e.g. nanotubes, in which portals essentially control selectivity.

<span class="mw-page-title-main">Host–guest chemistry</span> Supramolecular structures held together other than by covalent bonds

In supramolecular chemistry, host–guest chemistry describes complexes that are composed of two or more molecules or ions that are held together in unique structural relationships by forces other than those of full covalent bonds. Host–guest chemistry encompasses the idea of molecular recognition and interactions through non-covalent bonding. Non-covalent bonding is critical in maintaining the 3D structure of large molecules, such as proteins and is involved in many biological processes in which large molecules bind specifically but transiently to one another.

<span class="mw-page-title-main">Cryptand</span> Cyclic, multidentate ligands adept at encapsulating cations

In chemistry, cryptands are a family of synthetic, bicyclic and polycyclic, multidentate ligands for a variety of cations. The Nobel Prize for Chemistry in 1987 was given to Donald J. Cram, Jean-Marie Lehn, and Charles J. Pedersen for their efforts in discovering and determining uses of cryptands and crown ethers, thus launching the now flourishing field of supramolecular chemistry. The term cryptand implies that this ligand binds substrates in a crypt, interring the guest as in a burial. These molecules are three-dimensional analogues of crown ethers but are more selective and strong as complexes for the guest ions. The resulting complexes are lipophilic.

In chemistry, a non-covalent interaction differs from a covalent bond in that it does not involve the sharing of electrons, but rather involves more dispersed variations of electromagnetic interactions between molecules or within a molecule. The chemical energy released in the formation of non-covalent interactions is typically on the order of 1–5 kcal/mol. Non-covalent interactions can be classified into different categories, such as electrostatic, π-effects, van der Waals forces, and hydrophobic effects.

Co-solvents are defined as kosmotropic (order-making) if they contribute to the stability and structure of water-water interactions. In contrast, chaotropic (disorder-making) agents have the opposite effect, disrupting water structure, increasing the solubility of nonpolar solvent particles, and destabilizing solute aggregates. Kosmotropes cause water molecules to favorably interact, which in effect stabilizes intramolecular interactions in macromolecules such as proteins.

<span class="mw-page-title-main">Cation–π interaction</span>

Cation–π interaction is a noncovalent molecular interaction between the face of an electron-rich π system (e.g. benzene, ethylene, acetylene) and an adjacent cation (e.g. Li+, Na+). This interaction is an example of noncovalent bonding between a monopole (cation) and a quadrupole (π system). Bonding energies are significant, with solution-phase values falling within the same order of magnitude as hydrogen bonds and salt bridges. Similar to these other non-covalent bonds, cation–π interactions play an important role in nature, particularly in protein structure, molecular recognition and enzyme catalysis. The effect has also been observed and put to use in synthetic systems.

<span class="mw-page-title-main">Hofmeister series</span>

The Hofmeister series or lyotropic series is a classification of ions in order of their lyotrophic properties, which is the ability to salt out or salt in proteins. The effects of these changes were first worked out by Franz Hofmeister, who studied the effects of cations and anions on the solubility of proteins.

<span class="mw-page-title-main">Enzyme catalysis</span> Catalysis of chemical reactions by specialized proteins known as enzymes

Enzyme catalysis is the increase in the rate of a process by a biological molecule, an "enzyme". Most enzymes are proteins, and most such processes are chemical reactions. Within the enzyme, generally catalysis occurs at a localized site, called the active site.

Implicit solvation is a method to represent solvent as a continuous medium instead of individual “explicit” solvent molecules, most often used in molecular dynamics simulations and in other applications of molecular mechanics. The method is often applied to estimate free energy of solute-solvent interactions in structural and chemical processes, such as folding or conformational transitions of proteins, DNA, RNA, and polysaccharides, association of biological macromolecules with ligands, or transport of drugs across biological membranes.

<span class="mw-page-title-main">Molecular sensor</span>

A molecular sensor or chemosensor is a molecular structure that is used for sensing of an analyte to produce a detectable change or a signal. The action of a chemosensor, relies on an interaction occurring at the molecular level, usually involves the continuous monitoring of the activity of a chemical species in a given matrix such as solution, air, blood, tissue, waste effluents, drinking water, etc. The application of chemosensors is referred to as chemosensing, which is a form of molecular recognition. All chemosensors are designed to contain a signalling moiety and a recognition moiety, that is connected either directly to each other or through a some kind of connector or a spacer. The signalling is often optically based electromagnetic radiation, giving rise to changes in either the ultraviolet and visible absorption or the emission properties of the sensors. Chemosensors may also be electrochemically based. Small molecule sensors are related to chemosensors. These are traditionally, however, considered as being structurally simple molecules and reflect the need to form chelating molecules for complexing ions in analytical chemistry. Chemosensors are synthetic analogues of biosensors, the difference being that biosensors incorporate biological receptors such as antibodies, aptamers or large biopolymers.

In chemistry, π-effects or π-interactions are a type of non-covalent interaction that involves π systems. Just like in an electrostatic interaction where a region of negative charge interacts with a positive charge, the electron-rich π system can interact with a metal, an anion, another molecule and even another π system. Non-covalent interactions involving π systems are pivotal to biological events such as protein-ligand recognition.

In coordination chemistry, a stability constant is an equilibrium constant for the formation of a complex in solution. It is a measure of the strength of the interaction between the reagents that come together to form the complex. There are two main kinds of complex: compounds formed by the interaction of a metal ion with a ligand and supramolecular complexes, such as host–guest complexes and complexes of anions. The stability constant(s) provide(s) the information required to calculate the concentration(s) of the complex(es) in solution. There are many areas of application in chemistry, biology and medicine.

Lyotropy refers to concentration-dependent physical effects in solutions and often more specifically to ion-specific behavior in aqueous solutions.

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