Open access peer-reviewed chapter - ONLINE FIRST
Abstract
The erythrocyte membrane plays an important role in maintaining the structure, biological transport, and homeostasis of erythrocytes. The membrane consists of various unique proteins that serve specific functions. Band 3, an integral membrane protein of erythrocytes, constitutes about one-third of the membrane proteins. The amino-terminal region, positioned on the cytoplasmic side, comprises binding sites for hemoglobin, glycolytic enzymes, and ankyrin. Band 3 plays a crucial role in maintaining the structural integrity by connecting the lipid bilayer to the underlying cytoskeletal network. It has a versatile role in cellular dynamics, intracellular trafficking, cellular aging, gas exchange, cellular adhesion, and erythropoiesis. Oxidative modifications in band 3 can be detrimental to membrane structure, compromising its integrity, functionality, and cellular interactions. The intricate chemistry between band 3 and various cellular components unravels its significance in erythrocyte physiology and aging. Therefore, it can be employed as a potential molecular target for therapeutic interventions.
Keywords
- erythrocytes
- band 3
- cell membrane
- oxidative stress
- anion exchange
- AE1
1. Introduction
Erythrocytes constitute a significant portion of blood and have a distinctive role due to oxygen transport. These cells also facilitate the transport of carbon dioxide and thereby regulate blood pH [1]. Erythrocytes contain hemoglobin, which efficiently carries oxygen due to the affinity of heme group for oxygen. Hemoglobin undergoes breakdown on aging, resulting in the separation of iron and globin, which can be later recycled for the synthesis of new hemoglobin. This ensures continual regeneration and maintenance of oxygen-carrying function [2].
2. Erythrocyte membrane structure and function
Erythrocyte membrane is responsible for the antigenic transport and mechanical properties. It plays an important role in the intricate dynamics of erythrocyte biology. The membrane consists of two domains: lipid bilayer and cytoskeleton. The lipid bilayer consists of hydrophilic peripheral proteins internally, hydrophobic integral proteins in the middle (mainly band 3 and glycophorins), and external hydrophilic proteins. The cytoskeleton comprises specific peripheral proteins, including spectrin, ankyrin, actin, and Band 4.1R, 4.2 [1, 3].
Spectrin serves as the primary membrane protein in erythrocytes and exhibits self-associative properties. It forms a lattice structure in conjunction with other membrane proteins and actin, creating a supportive network on the inner aspect of the lipid bilayer. This lattice imparts unique properties of strength and elasticity to erythrocytes [4].
Ankyrin plays a crucial role in connecting the spectrin-actin cortical cytoskeleton with the cytoplasmic domains of integral membrane proteins. It forms a bridge between adhesion molecules and ion channels and integrates the structural and functional components of the erythrocyte membrane.
Glycophorins, also known as sialoglycoproteins, constitute approximately 2% of the total membrane protein in erythrocytes. These proteins are situated at the actin junctional complexes, acting as anchors that connect the cytoskeleton to the lipid bilayer. The amino terminals of glycophorins serve as the binding sites of antigens of ABO and MN blood groups. The inner carboxyl terminal faces the cytoplasm and interacts with the cytoskeleton [5].
2.1 Band 3 structure
Band 3 is an erythrocyte membrane protein with a molecular mass of 95 kDa, constituting about one-third of the membrane proteins. Band 3 is exposed on both membrane faces with a relatively low carbohydrate content (8% by weight). The amino-terminal region (41 kDa), positioned on the cytoplasmic side, contains a highly extended structure with binding sites for hemoglobin, glycolytic enzymes, and ankyrin [6].
Each unit of band 3 contains a single site for numerous stilbene disulfonate derivatives, which are potent inhibitors of anion transport. The membrane and cytoplasmic domains of adjacent subunits interact, forming band 3 dimers when the cytoplasmic domains are oxidatively cross-linked with cuprous ion and o-phenanthroline [7]. The cytoplasmic domain of band 3 differs among different species [8].
The carboxy terminus (52 kDa) is primarily composed of alpha-helical structures and arranged cylindrically, with multiple positively charged amino acids. These charges influence ion distribution across the membrane, repelling cations and attracting anions, thereby enhancing anion transport in both directions.
Various types of physical and biochemical evidence strongly suggest that band 3 exists as either a dimer or a tetramer within the membrane. Band 3 undergoes a monomer-dimer-tetramer equilibrium when isolated in non-ionic detergents. The predominant form of the protein is a dimer under normal conditions, with the possibility of tetramer formation [9].
2.2 Band 3 functions
Band 3 protein regulates various functions and plays a crucial role in maintaining erythrocyte stability and functional regulation. The band 3 region of the electrophoretic profile is recognized as anion exchanger 1 (AE1). Its functions include anion exchange-assisted oxygen transport, maintenance of structural integrity, regulating erythrocyte properties, formation of Wright (Wr) blood group antigen, and senescence. These functions may be influenced by its interactions with lipids or lipid domains in the plasma membrane [10].
2.2.1 Anion exchange
Erythrocytes are indispensable players in the exchange of gases within our bodies. The metabolically active cells can be distinguished from inactive ones by a combination of three mechanisms: the oxy/deoxy conversion of hemoglobin, carbonic anhydrase reaction, and the chloride shift.
Chloride shift, an anion exchange mechanism, crucial for delivering oxygen efficiently, is a result of synergy between hemoglobin, carbonic anhydrase, and the band 3 protein [11]. Carbon dioxide (CO2) produced in peripheral cells diffuses into the erythrocytes as they traverse through the capillaries. Carbonic anhydrase converts the diffused CO2 into bicarbonate (HCO3), triggering the chloride-bicarbonate exchange by the band 3 protein [12].
Anion exchange activity results in the conversion of weaker carbonic acid to stronger hydrochloric acid, inducing intracellular acidification. This transient effect facilitates the dissociation of oxygen from oxyhemoglobin (HbO2) in metabolically active cells. The concentration of carbon dioxide and acidity (Bohr effect) ensures that deoxyhemoglobin (HbH+) accepts protons, preventing further dissociation of oxygen from HbO2 [12].
Amino acid residues, including lysine, arginine, and glutamic acid, are known to be crucial for the anion exchange activity of band 3 protein [13]. Intracellular histidine residue of band 3 protein also participates in anion exchange [14].
2.2.2 Cytoskeletal interaction and structural integrity during erythropoiesis
Band 3 plays a crucial role in maintaining the structural integrity by connecting the lipid bilayer to the underlying cytoskeletal network in the early stages of erythroid differentiation. One of its primary functions is to form essential linkages with ankyrin, a cytoskeletal protein, thereby tethering the membrane to the spectrin-based skeletal network. Protein 4.2 modulates the interaction between band 3 and ankyrin during erythropoiesis [15].
The formation of a ternary junctional complex involving band 3, Rhesus-associated glycoprotein (RhAG), and other membrane proteins with protein 4.1R contributes significantly to membrane cohesion [15]. This complex, comprising β-spectrin and actin in the cytoskeleton, plays a vital role in maintaining the structural stability of the membrane throughout erythropoiesis. Interactions with additional cytoskeletal proteins, such as adducin and dematin, enhance the role of band 3 in connecting the bilayer to the membrane skeleton [16]. This is fundamental in preventing vesiculation and preserving the optimal surface area of the membrane.
2.2.3 Regulating glycolysis
Band 3 is also involved in the regulation of glycolysis. Glycolytic enzymes can bind to the cytoplasmic domain leading to inhibition. This can be reversed by phosphorylation of tyrosine 8 and/or 21 on band 3. It is a unique method of controlling glycolysis as it relies on reversible covalent inhibition. The inhibitory membrane binding site and the phosphorylation of specific tyrosine residues act as the regulators, influencing the activity of glycolytic enzymes [17].
2.2.4 Oxygen transport
Deoxyhemoglobin (deoxyHb) strongly and reversibly binds to band 3. This interaction acts like a molecular switch and can impact various erythrocyte functions based on oxygen levels. As oxygen increases, deoxyHb strengthens its association with band 3 and stabilizes the cell membrane [18, 19]. The flexible and unstructured nature of the amino terminus of band 3 provides an eightfold higher affinity to deoxyHb than to oxyhemoglobin (oxyHb) [20, 21, 22].
The association of glycolytic enzymes (GEs) on band 3 overlaps with the deoxyHb-binding site of the protein. DeoxyHb displaces GEs, thereby enhancing glucose consumption by glycolysis [23]. The central cavity being inaccessible upon Hb oxygenation allows the GEs to bind to the protein. This leads to a shift in glucose consumption from the pentose phosphate pathway at higher O2 levels to glycolysis at low O2 levels [23, 24].
2.2.5 Wright (Wr) blood group antigen formation
Band 3 plays a crucial role in the formation of the Wright (Wr) blood group antigen. The interaction between band 3 and glycophorin A (GPA) is vital to this process. The negatively charged phospholipids and cholesterol in erythrocyte membrane interact with band 3, creating an annulus around it. GPA interacts with band 3 outside of the Ankyrin complex to form the Wright blood group antigen [25]. This interaction is specific and involves the notable interaction of Glu658 in band 3 with Arg61 in GPA.
The GPA/band 3 complex, constituting the Wright blood group antigen, promotes the clustering of band 3 within the erythrocyte membranes. This complex formation is integral to the expression of the Wr blood group antigen in mature erythrocytes. Specific mutations, such as the Glu658Lys mutation, have been associated with the creation of the Wrb antigen [26].
2.2.6 Senescence
Senescence in erythrocytes includes biochemical, physical, conformational, and structural alterations mediated by oxidative and glycation events. Band 3 is critical to this phenomenon.
Tyrosine phosphorylation of band 3 by tyrosine kinase p72syk leads to cell dehydration and K+ efflux through the Gardos channel [27]. This is induced by Ca2+ (the Gardos effect) causing cell shrinkage leading to erythrocyte senescence [28].
In senescent erythrocytes, the breakdown of hemoglobin molecules results in the formation of hemichromes. This induces the clustering of nearby band 3 molecules on the cell surface and exposes concealed antigenic peptides (neo-antigens) on its surface [29, 30, 31]. The exposed antigen facilitates the recognition and targeting of senescent erythrocytes for their reticuloendothelial removal while hindering their endothelial adhesion. Fc receptor-dependent phagocytosis is a mechanism responsible for removing erythrocytes. These autoantibodies target a 62 kDa band 3 fragment found on senescent cells, emphasizing the importance of band 3 in the removal of senescent erythrocytes [32].
3. Oxidative stress
Oxidative stress (OS) is a physiological condition that occurs when there is an imbalance between the production of reactive oxygen species (ROS) and the body’s ability to detoxify or repair the damage caused by these highly reactive molecules. ROS, which includes free radicals like superoxide anion, hydroxyl radical, and non-radical species such as hydrogen peroxide, are natural byproducts of cellular metabolism. These are highly reactive and capable of causing damage to cellular structures [33].
Erythrocytes possess an efficient endogenous antioxidant system, consisting of superoxide dismutase, catalase, glutathione, peroxidase, peroxiredoxin-2, and glutathione [34]. Oxidative damage has been demonstrated to decrease erythrocyte survival and their rheological properties affecting their homeostasis [35, 36].
Band 3 protein can act as a marker of OS for the identification of specific oxidative modifications, such as cysteine oxidation. This is closely linked to band 3 protein, rendering it vulnerable to redox reactions [14, 37].
Band 3 modifications can impact the structure and function of erythrocytes.
Altered functionality: Oxidative modifications on band 3 can affect the anion exchange and transport capabilities of the membrane [37]. Elevated levels of ROS have been associated with OS and alterations in antioxidant defenses [38]. Oxidative reactions also induce Caspase-3 activation leading to the partial degradation of band 3 [39, 40].
Membrane integrity: Oxidative stress-induced modifications in band 3 may compromise the stability of the membrane. Erythrocytes activate tyrosine kinases during OS, causing tyrosine phosphorylation in the cytoplasmic domain of the band 3 protein. This phosphorylation mediates interactions with ankyrin, leading to membrane destabilization [41, 42].
Cell signaling: Band 3 is involved in cell signaling and interactions with other proteins. Oxidative stress-induced changes in band 3 could influence cell signaling pathways, leading to cellular responses and adaptations [37].
Cytoskeleton interaction: Band 3 interacts with the cytoskeleton, contributing to membrane stability. Oxidative modifications might interfere with these interactions, affecting the overall structure and shape of the cell [37]. Caspase-3 activation cleaves the cytoplasmic end of band 3, which disrupts its interactions with cytosolic proteins and interferes with its linkage to ankyrin [39]. These disruptions contribute to phosphatidylserine (PS) exposure, emphasizing the impact of OS, caspase-3 activation, band 3 alterations in erythrocyte deformability [39]. The intricate interplay of these molecular events underscores the multifaceted role of OS in shaping the biomechanical properties and physiological fate of erythrocytes.
Transport disruption: Band 3 plays a role in transporting ions across the membrane. Oxidant molecules circulating in the bloodstream exert their effects on the plasma membrane. They potentially impact the integrity of band 3 protein and, consequently, the transport systems [35, 36].
Cellular aging: Oxidation of band 3 has implications in the aging of erythrocytes. It contributes to the exposure of senescent-specific neo-antigens, which subsequently bind autologous immunoglobulin G (IgG), triggering the removal of erythrocytes from circulation. Moreover, the binding of IgG has been associated with the formation of band 3 clusters, initiated by the interaction of denatured oxidized hemoglobin (hemichromes) with band 3 [43, 44, 45].
4. Studies on band 3 protein
Studies focusing on the band 3 membrane protein in erythrocytes have been conducted, revealing valuable insights into its essential functions.
4.1 Enzymatic degradation of band 3
Enzymatic modifications of band 3 have provided interesting insights into its susceptibility to degradation. One specific enzyme, neutral proteases from erythrocyte membranes influenced by calcium ions, has a role in cleaving band 3 [46].
4.2 Role in gas exchange
Membrane proteins of band 3 anion exchanger (AE1) in erythrocytes in both mice and humans demonstrated the association of Rh-associated glycoprotein (RhAG) and Rh (a key part of gas channel) with band 3. Band 3 serves as the core of a macro complex comprising integral and peripheral membrane proteins. This macro complex plays a coordinated role as an integrated CO2/O2 gas exchange unit within the erythrocyte [47].
4.3 Implications in diseases
Band 3 has been identified as a major player in enhancing adhesion to endothelial cells in malaria-infected and sickle erythrocytes. Synthetic peptides derived from distinct regions of band 3, particularly from its outer parts, have demonstrated the ability to prevent abnormal adherence of sickle cells to endothelial cells. They show the significance of band 3 in mediating cellular interactions and provide potential therapeutic targets for conditions characterized by altered cell adhesion [48].
Band 3 protein plays a crucial role in erythrocyte homeostasis, particularly under hyperglycemic conditions associated with diabetes. The higher anion exchange capability in erythrocytes under hyperglycemia emphasizes band 3 protein’s sensitivity to glycated Hb levels and its impact on erythrocyte function [49].
4.4 Intracellular trafficking
The interaction between band 3 and Glycophorin A (GPA) was studied using transgenic mice producing human GPA. These form a close network in membrane stability and play a significant role in intracellular trafficking [50].
4.5 Pulmonary gas exchange
Contributions of band 3 to pulmonary gas exchange were studied in the canine models. Inhibition of Carbonic Anhydrase (CA) leads to a significant decrease in both CO2 and O2 showing a significant role of band 3 and carbonic anhydrase in pulmonary gas exchange. Erythrocyte membrane band 3 protein contributes to CA-catalyzed processes in pulmonary gas exchange [51].
The functions of band 3 are depicted in Figure 1.
Figure 1.
Comprehensive view of band 3 structure and functions.
5. Conclusion
Band 3 plays a versatile role in cellular dynamics, intracellular trafficking, and cellular aging, maintaining structural integrity, gas exchange, and cellular adhesion. Oxidative modifications to band 3 can have profound effects on membrane structure, compromising its integrity, functionality, and interactions with other cellular components. It serves a vital role in erythropoiesis. The intricate interplay between band 3 and various cellular components unravels its significance in erythrocyte physiology and aging. Band 3 has an integral role in maintaining erythrocyte homeostasis and cell integrity. Therefore, it can be employed as a potential molecular target for therapeutic interventions.
Acknowledgments
The authors acknowledge Masannagari Pallavi, Jennifer Margaret, and JAIN (Deemed-to-be University) for their support.
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