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3.A.1 The ATP-binding Cassette (ABC) Superfamily

The ABC superfamily contains both uptake and efflux transport systems, and the members of these two porter groups generally cluster loosely together with just a few exceptions (Saurin et al., 1999). ATP hydrolysis without protein phosphorylation energizes transport. There are dozens of families within the ABC superfamily, and family generally correlates with substrate specificity. However there are exceptions. The high resolution X-ray structures of several ABC transporters, both uptake and efflux systems, have been determined, and specific details of the transport mechanisms have been proposed (Davidson and Maloney, 2007; Lee et al., 2007). Several multidrug resistance (MDR) transporters catalyze lipid, lipopolysaccharide, and/or lipoprotein export. This can occur by a 'flip-flop' mechanism or a 'projection' mechanism (Nagao et al., 2010). Pagès et al. (2011) have described several classes of efflux pump inhibitors that counteract MDR. Known structures have been discussed by Zolnerciks et al. (2011) and by Wilkens 2015. Mechanistic models for the transport cycle have been compared (Szöllősi et al. 2017). Transporters can be modified posttranslationally by phsophorylation, ubiquitination, glycosylation and/or palmitoylation (Czuba et al. 2018). Ford and Beis 2019 reviewed  progress on structural determination of eukaryotic and bacterial ABC transporters as well as novel proposed mechanisms.  There are 48 genes encoding ABC transporters in humans (Sakamoto et al. 2019).  1,4-dihydropyridines are inhibitors of the transmembrane efflux pump ABCB1 in cancer cells, and they potentiate the inhibitory effect of clofazimine in Mycobacterium tuberculosis (Lentz et al. 2019). Phospholipids and cholesterol are inducers of cancer multidrug resistance and therapeutic targets (Kopecka et al. 2019). Multiple positions (residues) in the membrane domains of ABC transporters influence their substrate selectivities (Srikant et al. 2020). An involvement of ABC porters in cancer multidrug resistance (MDR) has been reviewed (Juan-Carlos et al. 2021). The functional dynamics (substrate transport) of ABC transporters are realized by concerted motions, such as NBD dimerization, mechanical transmission via coupling helices, and the translocation of substrates through TMDs, which are induced by the binding and/or hydrolysis of ATP molecules and substrates (Furuta 2021). Automatic algorithms have been derived that permit the large-scale identification of the solute binding protein (SBP) repertoire in proteomes (Ortega et al. 2022).  An alternating access mechanism for many bacterial and mammalian ABC-type multidrug resistance (MDR) transporters has been reviewed (Badiee et al. 2023). It has been proposed that ATP binding cassette transporters  evolved roles in herbicide resistance through exaptation (Caygill and Dolan 2023).

Switch and constant contact models have been presented (George and Jones, 2012).  The prevailing paradigm for the ABC transport mechanism is the Switch Model, in which the nucleotide binding domains are proposed to dimerise upon binding of two ATP molecules, and thence dissociate upon sequential hydrolysis of the ATP. This idea appears consistent with crystal structures of both isolated subunits and whole transporters, as well as with the biochemical data. Nonetheless, an alternative Constant Contact Model has been proposed, in which the nucleotide binding domains do not fully dissociate, and ATP hydrolysis occurs alternately at each of the two active sites (Jones and George 2012).  In this model, one of the sites remains closed and contains an occluded nucleotide at all times. The cassettes remain in contact, and the active sites swing open in an alternately seesawing motion. Whilst the concept of NBD association/dissociation in the Switch Model is naturally compatible with a single alternating-access channel, the asymmetric functioning proposed by the Constant Contact model suggests an alternating or reciprocating function in the TMDs. A new model for the function of ABC transporters has been proposed by Jones and George 2014 in which the sequence of ATP binding, hydrolysis, and product release in each active site is directly coupled to the analogous sequence of substrate binding, translocation and release in one of two functionally separate substrate translocation pathways. Each translocation pathway functions 180 degrees out of phase.

As noted above, the porters of the ABC superfamily consist of two integral membrane domains/proteins and two cytoplasmic domains/proteins. The uptake systems (but not the efflux systems) usually possess extracytoplasmic solute-binding receptors (one or more per system) which in Gram-negative bacteria are found in the periplasm, and in Gram-positive bacteria is present either as a lipoprotein, tethered to the external surface of the cytoplasmic membrane, or as a cell surface-associated protein, bound to the external membrane surface via electrostatic interactions. For those systems with two or more extracytoplasmic solute binding receptors, the receptors may interact in a cooperative fashion (Biemans-Oldehinkel and Poolman, 2003). These binding proteins fall into six phylogenetic clusters (Berntsson et al., 2010). Both the integral membrane channel constituent(s) and the cytoplasmic ATP-hydrolyzing constituent(s) may be present as homodimers or heterodimers. Two families of ABC transporters have members in which one or two receptors are fused to either the N- or C-terminus of the translocating membrane protein. This suggests that two or even four substrate-binding sites may function in the complex. Possibly multiple receptors in proximity to the translocator enhances the transport rate. Multiple receptors may also broaden the substrate specificity of the system (van der Heide and Poolman, 2002). These systems with covalent receptor domains linked to the transmembrane translocators are found in the PAAT family (TC #3.A.1.3) and the QAT family (TC #3.A.1.12) (van der Heide and Poolman, 2002). Some high affinity ABC uptake systems specific for vitamins, minerals and other small molecules, called ECF systems, lack an extracytoplasm receptor and function by a mechanisms as discussed by Slotboom 2014. Both ECF (type I) and binding protein receptor-dependent uptake systems have been found in eukaryotes, especially in chloroplasts of algae and lower plants (Choi and Ford 2021). The diversity of ABC transporter genes across the phylum Nematoda has been examined (Langeland et al. 2021). Most of the ABCB and ABCG subfamily members are actively involved in heavy metal responses, and the functions of specific ABC transporters in Cd2+ and Hg2+ stress responses is likely in soybean (Glycine max L.) (Naaz et al. 2023). Some ABCG transporters in plants are likely to transport plant terpenes (Salgado et al. 2023).

ABC transporters always have two nucleotide binding domains (NBDs or NBSs). ATP-bound NBDs dimerize in a head-to-tail arrangement, with two nucleotides sandwiched at the dimer interface. Upon the binding of ATP molecules to nucleotide binding domains (NBDs), ATP-binding cassette (ABC) exporters undergo a conformational transition from an inward-facing (IF) to an outward-facing (OF) state via chemo-mechanical coupling. The ATP binding energy is converted into distortion energy of several transmembrane helices (Arai et al. 2017). Both NBDs contribute residues to each of the two nucleotide-binding sites (NBSs) in the dimer. The prototypical NBD MJ0796 from Methanocaldococcus jannaschii forms ATP-bound dimers that dissociate completely following hydrolysis of one of the two bound ATP molecules.  ATP hydrolysis at one nucleotide-binding site drives NBD dissociation, but two binding sites are required to form the ATP-sandwich NBD dimer necessary for hydrolysis (Zoghbi and Altenberg 2013). Single versus dimeric subunit ATPase have been discussed (Ford and Hellmich 2020). Transporters with two active NBSs are called canonical transporters, while ABC exporters from eukaryotic organisms frequently have a degenerate NBS1 containing noncanonical residues that strongly impair ATP hydrolysis. The latter have been reviewed (Stockner et al. 2020). A summary of the structures available and an overview of recent structure-based studies have been discussed, while the artificial intelligence (AI)-based predictions from AlphaFold-2 are considered (Huang and Ecker 2023). Eight families of MDR effux pump inhibitors, active against Escherichia coli or Pseudomonas aeruginosa have been described and reviewed (Compagne et al. 2023).  A total of 159 ABC genes were identified in the legume, Cajanus cajan, that belong to eight canonical classes, CcABCA to CcABCG and CcABCI (Mall et al. 2023). Different cis-acting regulatory elements like stress, hormone, and cellular responsive were identified, and expression profiling of CcABC genes at various developmental stages of different anatomical tissues was performed.

Kinases can affect the activities of ABC transporters as do protein-protein interactions. Crawford et al. 2018 reviewed the effects of such interactions on the ABC transporters ABCB1, ABCB11, ABCC1, ABCC4, and ABCG2 of humans, showing how kinases and protein-protein interactions regulate these transporters. Yeast have all of these types of ABC transporters, and a comprehensive overview of these proteins of the drug-resistant human fungal pathogen, Candida glabrata (Kumari et al. 2018). A comprehensive review of the classes of efflux pump inhibitors from various sources, highlighting their structure-activity relationships, which can be useful for medicinal chemists in the pursuit of novel efflux pump inhibitors has appeared (Durães et al. 2018). Protein expression and functional relevance of various primary and secondary drug efflux and uptake porters at the Blood-Brain Barrier of human brain and glioblastoma have been investigated (Bao et al. 2019). ABC transporter gene expression and mutational status not surprisingly affect survival rates of cancer patients (Kadioglu et al. 2020). Copper N-(2-hydroxy acetophenone) glycinate (CuNG) exerted different modulatory activities towards ABC-transporter-expressing cells. While CuNG-mediated ABC-transporter inhibition may improve tumor chemotherapy, CuNG-mediated enhanced ABC-transport may be a new strategy to ameliorate inflammatory diseases associated with decreased ABC-transporter expression as in ulcerative colitis (Hartinger et al. 2023).

Acar et al. 2020 investigated the allosteric networks of three representative ABC transporters using a hybrid molecular simulations approach validated by experiments. Each of the three transporters uses a different allosteric network. In the constitutive B12 importer BtuCD, ATP binding is the main driver of allostery and docking/undocking of the substrate-binding protein (SBP), which is the driven event. The allosteric signal originates at the cytoplasmic side of the membrane before propagating to the extracellular side. In the substrate-controlled maltose transporter, the SBP is the main driver of allostery, ATP binding is the driven event, and the allosteric signal propagates from the extracellular to the cytoplasmic side of the membrane. In the lipid flippase PglK, a cyclic crosstalk between ATP and substrate binding underlies allostery. These results demonstrate that speciation of biological functions may arise from variations in allosteric connectivity (Acar et al. 2020).

Using mass spectrometry, Al-Majdoub et al. 2020 identified and quantified the amounts of 32 (out of 48) ABC transporters in several human tissues. ABCD3 was the most abundant in liver, whereas ABCA8, ABCB2/TAP1, and ABCE1 were detected in all tissues.They created an atlas which revealed that ABCB2/TAP1 may have TAP2-independent functions in the brain, and that livers from biliary atresia patients have quite different ABC-transporter profiles than controls. Nearly a third to half of patients with noninfectious uveitis (NIU) fail to achieve control with immunomodulatory therapy due to MDR (Tagirasa et al. 2020). Rapid-onset obesity with hypothalamic dysfunction, hypoventilation, and autonomic dysregulation (ROHHAD) syndrome is a rare neurocristopathy.  ATPase transmembrane transporters, acetylglucosaminyltransferases, and phagocytic vesicle membrane proteins may contribute to the ROHHAD phenotype (Victor et al. 2023).  Mutations in ABC genes cause 21 monogenic diseases, and polymorphisms in these genes are associated with susceptibility to complex diseases (Duvivier et al. 2024). ABC transporters also play a major role in drug bioavailability, and they mediate multidrug resistance in cancer. At least 13 ABC transporters were shown to be involved in drug resistance in vitro.

The involvement of ABC transporters in transport of secondary metabolites in medicinal plants has been reviewed (Liu et al. 2021). 49 ABC transporter genes have been divided into eight subfamilies (ABCA-ABCH), including seven ABCAs, seven ABCBs, 10 ABCCs, two ABCDs, one ABCE, three ABCFs, 16 ABCGs, and three ABCHs according to phylogenetic analysis in Zeugodacus cucurbitae, a highly destructive insect pest of cucurbitaceous and other related crops (Xu et al. 2021). Transporter-mediated natural product-drug interactions have been reviewed for transporters in several different families (Bi et al. 2022). The new AlphaFold protein structure prediction tool predicts a new type of transmembrane domain fold within the ABC transporters that is associated with cation exporters of bacteria and plants (Younus et al. 2022).

Plant MRPs, or GS-X pumps (glutathione-conjugate or multispecific organic anion Mg2+-ATPases,  participate in the transport of exogenous and endogenous amphipathic anions and glutathionated compounds, usually from the cytosol into the vacuole. Encoded by a multigene family and possessing a unique domain organization, the types of processes that likely converge and depend on plant MRPs include herbicide detoxification, cell pigmentation, the alleviation of oxidative damage, and the storage of antimicrobial compounds. Additional functional capabilities might include channel regulation of activity and/or the transport of heavy metal chelates (Rea et al. 1998).

The TC system of classification uses the integral membrane proteins, not the energy coupling proteins, receptor, or auxiliary subunits to classify the system into families (Saier, 1994; 2000). The exception to this rule was the ABC superfamily which by engrained tradition was classified based on the use of an ATP-binding cassette (ABC) ATPase for energy coupling before the TC system was designed. Since then it has become known that the membrane proteins of ABC export systems fall into three evolutionarily distinct families that followed three different pathways of origin (Wang et al., 2009). These have been designated ABC1, ABC2 and ABC3. ABC1 porters arose by triplication of a primordial 2 TMS element; ABC2 porters arose by duplication of a 3 TMS element, and ABC3 porters arose from a 4 TMS precursor that either remained as two 4 TMS proteins (a homo or hetero dimer) or internally duplicated to give 8 or 10 proteins, the extra two appear to be in the center between the two 4 TMS repeat units (Khwaja et al. 2005). The ABC functional superfamily therefore consists of at least three true superfamilies. The ABC subfamiies or clusters that belong to each of these three superfamilies are listed below. In addition, the LPS effluxing transport system family with TC# 3.A.152 may be unrelated to the other three exporter superfamilies (Thomas et al. 2020). Based on 3-D structures, there may also be three types of integral membrane ABC uptake systems, bringing the total to 7 types (Thomas et al. 2020).

Energy-coupling factor (ECF)-type ABC importers appear to fulfil important roles in both algae and plants where they form the ABCI sub-family. Choi and Ford 2021 discussed whether bacterial Type I and Type II ABC importers are present in extant eukaryotes. Type I importers exist in algae and the liverwort family of primitive non-vascular plants, but not in higher plants. The existence of eukaryotic Type II importers is also supported: a transmembrane protein homologous to vitamin B12 import system transmembrane protein (BtuC), hemin transport system transmembrane protein (HmuU) and high-affinity zinc uptake system membrane protein (ZnuB) is encoded within the Cyanophora paradoxa genome. This last protein has homologs within the genomes of red algae. Furthermore, its candidate nucleotide-binding domain (NBD) shows closest similarity to other bacterial Type II importer NBDs such as BtuD. Functional studies suggest that Type I importers have roles in maintaining sulphate levels in the chloroplast, while Type II importers probably act as importers of Mn2+ or Zn2+ , as inferred by comparisons with bacterial homologs. Possible explanations for the presence of these transporters in simple plants, but not in other eukaryotic organisms, are considered (Choi and Ford 2021). In order to utilise the existing nomenclature for eukaryotic ABC proteins, it was proposed that eukaryotic Type I and II importers be classified as ABCJ and ABCK transporters, respectively.

3.A.1.106 The Lipid Exporter (LipidE) Family
3.A.1.108 The β-Glucan Exporter (GlucanE) Family
3.A.1.109 The Protein-1 Exporter (Prot1E) Family
3.A.1.110 The Protein-2 Exporter (Prot2E) Family
3.A.1.111 The Peptide-1 Exporter (Pep1E) Family
3.A.1.112 The Peptide-2 Exporter (Pep2E) Family
3.A.1.113 The Peptide-3 Exporter (Pep3E) Family
3.A.1.117 The Drug Exporter-2 (DrugE2) Family
3.A.1.118 The Microcin J25 Exporter (McjD) Family
3.A.1.119 The Drug/Siderophore Exporter-3 (DrugE3) Family
3.A.1.123 The Peptide-4 Exporter (Pep4E) Family
3.A.1.127 The AmfS Peptide Exporter (AmfS-E) Family
3.A.1.129 The CydDC Cysteine Exporter (CydDC-E) Family
3.A.1.135 The Drug Exporter-4 (DrugE4) Family
3.A.1.139 The UDP-Glucose Exporter (U-GlcE) Family (UPF0014 Family)
3.A.1.201 The Multidrug Resistance Exporter (MDR) Family (ABCB)
3.A.1.202 The Cystic Fibrosis Transmembrane Conductance Exporter (CFTR) Family (ABCC)
3.A.1.203 The Peroxysomal Fatty Acyl CoA Transporter (P-FAT) Family (ABCD)
3.A.1.206 The a-Factor Sex Pheromone Exporter (STE) Family (ABCB)
3.A.1.208 The Drug Conjugate Transporter (DCT) Family (ABCC) (Dębska et al., 2011)
3.A.1.209 The MHC Peptide Transporter (TAP) Family (ABCB)
3.A.1.210 The Heavy Metal Transporter (HMT) Family (ABCB)
3.A.1.212 The Mitochondrial Peptide Exporter (MPE) Family (ABCB)
3.A.1.21   The Siderophore-Fe3+ Uptake Transporter (SIUT) Family

3.A.1.101 The Capsular Polysaccharide Exporter (CPSE) Family
3.A.1.102 The Lipooligosaccharide Exporter (LOSE) Family
3.A.1.103 The Lipopolysaccharide Exporter (LPSE) Family
3.A.1.104 The Teichoic Acid Exporter (TAE) Family
3.A.1.105 The Drug Exporter-1 (DrugE1) Family
3.A.1.107 The Putative Heme Exporter (HemeE) Family
3.A.1.115 The Na+ Exporter (NatE) Family
3.A.1.116 The Microcin B17 Exporter (McbE) Family
3.A.1.124 The 3-component Peptide-5 Exporter (Pep5E) Family
3.A.1.126 The β-Exotoxin I Exporter (βETE) Family
3.A.1.128 The SkfA Peptide Exporter (SkfA-E) Family
3.A.1.130 The Multidrug/Hemolysin Exporter (MHE) Family
3.A.1.131 The Bacitracin Resistance (Bcr) Family
3.A.1.132 The Gliding Motility ABC Transporter (Gld) Family
3.A.1.133 The Peptide-6 Exporter (Pep6E) Family
3.A.1.138 The Unknown ABC-2-type (ABC2-1) Family
3.A.1.141 The Ethyl Viologen Exporter (EVE) Family (DUF990 Family)
3.A.1.142 The Glycolipid Flippase (G.L.Flippase) Family
3.A.1.143 The Exoprotein Secretion System (EcsAB(C))
3.A.1.144:  Functionally Uncharacterized ABC2-1 (ABC2-1) Family
3.A.1.145:  Peptidase Fused Functionally Uncharacterized ABC2-2 (ABC2-2) Family
3.A.1.146:  The actinorhodin (ACT) and undecylprodigiosin (RED) exporter (ARE) family
3.A.1.147:  Functionally Uncharacterized ABC2-2 (ABC2-2) Family
3.A.1.148:  Functionally Uncharacterized ABC2-3 (ABC2-3) Family
3.A.1.149:  Functionally Uncharacterized ABC2-4 (ABC2-4) Family
3.A.1.150:  Functionally Uncharacterized ABC2-5 (ABC2-5) Family
3.A.1.151:  Functionally Uncharacterized ABC2-6 (ABC2-6) Family
3.A.1.152:  The lipopolysaccharide export (LptBFG) Family
3.A.1.204 The Eye Pigment Precursor Transporter (EPP) Family (ABCG)
3.A.1.205 The Pleiotropic Drug Resistance (PDR) Family (ABCG)
3.A.1.211 The Cholesterol/Phospholipid/Retinal (CPR) Flippase Family (ABCA)
9.B.74      The Phage Infection Protein (PIP) Family

3.A.1.114 The Probable Glycolipid Exporter (DevE) Family
3.A.1.122 The Macrolide Exporter (MacB) Family
3.A.1.125 The Lipoprotein Translocase (LPT) Family
3.A.1.134 The Peptide-7 Exporter (Pep7E) Family
3.A.1.136 The Uncharacterized ABC-3-type (U-ABC3-1) Family
3.A.1.137 The Uncharacterized ABC-3-type (U-ABC3-2) Family
3.A.1.140 The FtsX/FtsE Septation (FtsX/FtsE) Family
3.A.1.207 The Eukaryotic ABC3 (E-ABC3) Family

Uptake systems (TC#s 3.A.1.1 - 3.A.1.34) may be largely of the ABC2 type, but they have undergone extensive sequence and topological diversification. They even have different 3-dimensional structural differences, suggesting that they may have different origins. The only exception is ABC family 3.A.1.21, the Siderophore-Fe3+ Uptake Transporter (SIUT) Family which is clearly of the ABC1 type. It has no extracytoplasmic receptor as well. 

ABC importers have been divided into two classes: type I importers follow an alternating access mechanism driven by the presence of the substrate, while type II importers accept substrates in a nucleotide-free state, with hydrolysis driving an inward-facing conformation.  RbsABC2 (TC#3.A.1.2.1) seems to share functional traits with both type I and type II importers, as well as possessing unique features, and may employ a distinct mechanism relative to other ABC transporters (Clifton et al. 2014).

Unlike most uptake systems which have one or two functionally equivalent membrane subunits that form a homo- or hetero-dimer and an extracytoplasmic receptor, a subset of these porters have two functionally dissimilar membrane subunits, called S (substrate recognition) and T (energy transducer) that are very divergent in sequence, and they lack extracytoplasmic receptors (Erkens et al. 2012). This group of ABC porters represent a subfamily within the ABC uptake systems. This subset, called Energy-coupling Factor 'ECF' porters, includes:

3.A.1.18 The Cobalt Uptake Transporter (CoT) Family 
3.A.1.22 The Nickel Uptake Transporter (NiT) Family
3.A.1.23 The Nickel/Cobalt Uptake Transporter (NiCoT) Family
3.A.1.25 The Biotin Uptake Transporter (BioMNY) Family
3.A.1.26 The Putative Thiamine Uptake Transporter (ThiW) Family
3.A.1.28 The Queuosine (Queuosine) Family
3.A.1.29 The Methionine Precursor (Met-P) Family
3.A.1.30 The Thiamin Precursor (Thi-P) Family
3.A.1.31 The Unknown-ABC1 (U-ABC1) Family
3.A.1.32 The Cobalamin Precursor (B12-P) Family
3.A.1.33 The Methylthioadenosine (MTA) Family
S-subunits are homologous to:
2.A.87 The Prokaryotic Riboflavin Transporter (P-RFT) Family
2.A.88 The Vitamin Uptake Transporter (VUT or ECF) Family

Karpowich and Wang (2013) characterized the ECF transporters from Thermotoga maritima and Streptococcus thermophilus and determined a subunit stoichiometry of 2S:2T:1A:1A'.  They concluded that S subunits for different substrates can be incorporated into the same transporter complex simultaneously. In the crystal structure of the A-A' heterodimer, each subunit contains a novel motif called the Q-helix that plays a role in subunit coupling with the T subunits. A mechanism for coupling ATP binding and hydrolysis to transmembrane transport by ECF transporters was proposed. ECF porters mediate the uptake of micronutrients in prokaryotes, and consist of two ATP-binding-cassette family ATPases, a transmembrane coupling protein (T component) and a substrate-binding membrane protein (S component), as noted above. ECF transporters for Co2+ and Ni2+ ions have one or two additional proteins with extracytoplasmic regions. Homologs of T components with predicted localization in plastids are widespread in plants, but S components in eukaryotes are rare and restricted to biotin-specific variants (Finkenwirth and Eitinger 2019). Apart from a potential contribution to the export of flavins to serve the assembly of extracytoplasmic electron transfer chains, ECF transporters function as importers.

The maltose import transporter is composed of two TM subunits, MalF and MalG, and two subunits of a cytoplasmic ATPase, MalK. Like many uptake systems in Gram-negative bacteria, the periplasmic maltose-binding protein (MBP), is required to stimulate the ATPase activity of the transporter. In the absence of maltose, MBP exists in equilibrium between an open and closed conformation, and binding of maltose stabilizes the closed conformation. Two structures of MalFGK2 have been determined by x-ray crystallography. In the absence of MBP, MalFGK2 forms an inward-facing conformation with the TM maltose-binding site exposed to the cytoplasm. An outward-facing conformation, crystallized in complex with open MBP and ATP, shows that closure of the NBDs of MalK is concomitant with transfer of maltose from MBP to the TM subunits. These structures capture two states in the transport cycle: The inward-facing conformation represents the resting state where the transporter has a very low ATPase activity, and the outward-facing conformation represents a catalytic intermediate where ATP is poised for hydrolysis. Because MBP stimulates ATP hydrolysis and initiates the transport process, it must interact with the resting state conformation to form a 'pretranslocation' complex that is metastable in order to advance to the outward-facing conformation in the presence of ATP (25). Oldham and Chen (2011) presented the crystal structure of the initial complex formed between closed MBP and MalFGK2. As an essential intermediate between the inward- and outward-facing conformations, this structure suggests a mechanism by which substrate bound on the periplasmic surface influences the conformation of the NBDs at the intracellular surface. The same investigators suggested that ABC transporters catalyze ATP hydrolysis via a general base mechanism (Oldham and Chen, 2011).

The homodimeric LmrA drug efflux pump (TC #3.A.1.117.1) of Lactococcus lactis appears to function by an alternating site (half of sites) type mechanism. In many of these porters, the various domains are fused in a variety of combinations. Uptake porters generally have their constituents as distinct polypeptide chains, while efflux systems usually have them fused. ABC-type uptake systems have not been identified in eukaryotes, but ABC-type efflux systems abound in both prokaryotes and eukaryotes. The eukaryotic efflux systems often have the four domains (two cytoplasmic domains and two integral membrane domains) fused into either one or two polypeptide chains. The integral membrane porter domains each usually possesses 5 (uptake) or 6 (efflux) transmembrane spanners, but exceptions exist. For example, the MntB protein (TC #3.A.1.15.1) exhibits 9 established TMSs. The 3-dimensional structure of the E. coli MsbA protein (TC #3.A.1.106.1) has been solved to a resolution of 3.7 Å (Ward et al., 2007), that of the Staphylococcus aureus Sav1866 protein (TC #3.A.1.106.2) has been solved to a resolution of 3.0 Å (Dawson and Locher, 2006), that of the Archaeoglobus fulgidus ModABC complex has been solved at 3.1 Å resolution (Hollenstein et al., 2007), that of the E. coli BtuCDF Vitamin B12 transporter was solved at 2.6 Å resolution (Hvorup et al., 2007), and the maltose transporter has been solved at 2.8 Å resolution (Oldham et al., 2007). These structures are very different, but the two transmembrane domains form a single barrel 5-6 nm in diameter and about 5 nm deep with an entral pore open either to the external or internal surface spanning much of the membrane (Rosenberg et al., 2003). A model has been proposed allowing the channel to open up to the lipid bilayer. A half of sites model in which the two nucleotide binding domains interact in a fashion controlled by substrate binding has also been proposed (Hou et al., 2003; Loo et al., 2003).

Hollenstein et al. (2007) presented the 3.1 Å crystal structure of a putative molybdate transporter (ModB2C2) from Archaeoglobus fulgidus in complex with its binding protein (ModA). Twelve transmembrane helices of the ModB subunits provide an inward-facing conformation, with a closed gate near the external membrane boundary. The ATP-hydrolyzing ModC subunits reveal a nucleotide-free, open conformation, whereas the attached binding protein aligns the substrate-binding cleft with the entrance to the presumed translocation pathway. Structural comparison of ModB2C2A with Sav1866 suggests a common alternating access and release mechanism, with binding of ATP promoting an outward-facing conformation and dissociation of the hydrolysis products promoting an inward-facing conformation. ATP hydrolysis at one of the two sites in ABC transporters initiates transport-related conformational transitions (Gyimesi et al., 2011).

Smriti et al., 2009 mapped residues proximal to the daunorubicin (DNR)-binding site in MsbA (TC#3.A.1.106.1) using site-specific, ATP-dependent quenching of DNR intrinsic fluorescence by spin labels. In the nucleotide-free MsbA intermediate, DNR-binding residues cluster at the cytoplasmic end of helices 3 and 6 at a site accessible from the membrane/water interface and extending into an aqueous chamber formed at the interface between the two transmembrane domains. Binding of a nonhydrolyzable ATP analog inverts the transporter to an outward-facing conformation. DNR may thus enter near an elbow helix parallel to the water/membrane interface, partitioning into the open chamber, and then translocating toward the periplasm upon ATP binding.

The turnover rates of some transporters are inhibited by their substrates in a process termed trans-inhibition. Gerber et al. (2008) presented the crystal structure of a molybdate/tungstate ABC transporter (ModBC) from Methanosarcina acetivorans in a trans-inhibited state. The regulatory domains of the nucleotide-binding subunits proved to be in close contact, providing two oxyanion binding pockets at the shared interface. By specifically binding to these pockets, molybdate or tungstate prevent adenosine triphosphatase activity and lock the transporter in an inward-facing conformation, with the catalytic motifs of the nucleotide-binding domains separated. This allosteric effect prevents the transporter from switching between the inward-facing and the outward-facing states, thus interfering with the alternating access and release mechanism.

The cystic fibrosis transmembrane conductance regulator (CFTR; 3.A.1.202.1) is an ATP-dependent chloride channel. Jordan et al., 2008 compared CFTR protein sequences to those of ABCC4 proteins (the closest mammalian paralogs) to identify the evolutionary transition from transporter to channel activity. R352 in the sixth transmembrane helix interacts with D993 in TM9 to stabilize the open-channel state; D993 is absolutely conserved between CFTRs and ABCC4s. Thus CFTR channel activity evolved, at least in part, by converting the conformational changes associated with binding and hydrolysis of ATP, as are found in true ABC transporters, into an open permeation pathway by means of intraprotein interactions that stabilize the open state.  In general, plant ABC transport systems are more numerous than those in animals.  The maize systems have been categorized and their expression profiles have been determined (Pang et al. 2013).

The LolCDE complex of Escherichia coli (TC# 3.A.1.125.1) initiates the lipoprotein sorting to the outer membrane by catalysing their release from the inner membrane. LolC and/or LolE, membrane subunits, recognize lipoproteins anchored to the outer surface of the inner membrane, while LolD hydrolyses ATP on its inner surface. The ligand-bound LolCDE has been purified from the inner membrane in the absence of ATP (Ito et al., 2006). Liganded LolCDE represents an intermediate of the release reaction and exhibits higher affinity for ATP than the unliganded form. ATP binding to LolD weakens the interaction between LolCDE and lipoproteins and causes their dissociation in a detergent solution, while lipoprotein release from membranes requires ATP hydrolysis. A single molecule of lipoprotein is found to bind per molecule of the LolCDE complex.

The three structurally dissimilar constituents of the ABC uptake porters have generally arisen from a common ancestral porter system with minimal shuffling of constituents between/domain constituents is almost always the same. However the rates of sequence divergences differ drastically with the extracytoplasmic solute-binding receptors diverging most rapidly, the integral-membrane, channel-forming constituents diverging at an intermediate rate, and the cytoplasmic ATP-hydrolyzing constituents diverging most slowly. Thus, all ATP-hydrolyzing constituents are demonstrably homologous, but this is not true for the integral membrane constituents or the receptors. Nevertheless, clustering patterns are generally the same for all three types of proteins, and 3-dimensional structural data suggest that, in spite of their extensive sequence divergence, the extracytoplasmic solute-binding receptors are homologous to each other.

Unlike most of the known ABC transporters, ABCC1 (TC #3.A.1.208.8) has an additional membrane-spanning domain (MSD) at its amino terminus with a domain arrangement of MSD0-MSD1-NBD1-MSD2-NBD2. The additional MSD0 domain consists of five putative transmembrane segments with a predicted extracellular amino terminus. It has a U-shaped folding with the bottom of the U-structure facing cytoplasm and both ends in extracellular space. This U-shaped amino terminus probably functions as a gate to regulate the drug transport activity of human ABCC1 (Chen et al., 2006).

Polar lipid trafficking is essential in eukaryotic cells as membranes of lipid assembly are often distinct from final destination membranes. A striking example is the biogenesis of the photosynthetic membranes (thylakoids) in plastids of plants. Lipid biosynthetic enzymes at the endoplasmic reticulum and the inner and outer plastid envelope membranes are involved. This compartmentalization requires extensive lipid trafficking. Mutants of Arabidopsis disrupt the incorporation of endoplasmic reticulum-derived lipid precursors into thylakoid lipids. Two proteins affected in two of these mutants, trigalactosyldiacylglycerol 1 (TGD1) and TGD2, encode the permease and substrate binding component, respectively, of a proposed lipid translocator at the inner chloroplast envelope membrane. A third protein, TGD3, a small ABC-type ATPase, energizer transport. As in the tgd1 and tgd2 mutants, triacylglycerols and trigalactolipids accumulate in a tgd3 mutant. The TGD3 protein shows basal ATPase activity and is localized inside the chloroplast beyond the inner chloroplast envelope membrane. Proteins orthologous to TGD1, -2, and -3 are predicted to be present in Gram-negative bacteria, and the respective genes are organized in operons suggesting a common biochemical role for the gene products. The Tgd1,2,3 system (TC#3.A.1.27.2) probably transfers ER-derived lipids to the thylakoid membrane (Lu et al., 2007). It is one of the few known eukaryotic uptake systems.

Rodionov et al., 2009 identified 21 families of these substrate capture proteins, each with a different specificity predicted by genome context analyses. Roughly half of the substrate capture proteins (335 cases) examined by Rodionov et al., 2009 have a dedicated energizing module, but in 459 cases distributed among almost 100 gram-positive bacteria, different and unrelated substrate capture proteins share the same energy-coupling module. The shared use of energy-coupling modules was experimentally confirmed for folate, thiamine, and riboflavin transporters. Rodionov et al., 2009 proposed the name energy-coupling factor transporters for the new class of putative ABC membrane transporters. These membrane proteins are homologues to ABC-2 exporters. When evidence is minimal for association with an ABC-type ATP-hydrolyzing subunit, these porters are placed in category 2.A (secondary carriers; e.g., 2.A.88).

Canonical ABC importers play important roles in cell integrity, environmental stresses, cell-to-cell communication, cell differentiation and pathogenicity. An ABC sub-superfamily of micronutrient importers, the 'energy-coupling factor' (ECF) transporters, use ABC ATPases. Fundamental differences between tranditional ABC and ECF porters include the modular architecture and the independence of ECF systems of extracytoplasmic solute-binding proteins. Eitinger et al. (2011) review the roles of both types of transporters in diverse physiological processes including pathogenesis. They also point out the differences and similarities in modular assembly and their traits.

The uptake porters of the ABC superfamily and of the vitamin/small molecule transporters described by Rodionov et al., 2009 are homologous to the porters in the VUT family (2.A.88). In fact, studies indicated that all uptake porters of the ABC superfamily are of the ABC2 type (Zheng et al. 2013). When evidence suggests that homologous membrane transport proteins of the ABC2 type couple transport to ATP hydrolysis using a homologue of the ABC-type ATPases, we list these proteins in the ABC superfamily. If there is no such evidence, (e.g., experimental evidence and the occurrence of the gene for the membrane transporter protein is in an operon that lacks the ATPase and auxillary subunit) then the porter is placed into family 2.A.88.

Ter Beek et al. (2011) have determined the subunit stoichiometry and functional unit of the energy coupling factor (ECF)-type of ABC transporters (Rodionov et al., 2009). ECF transporters consist of a conserved energizing module (two peripheral ATPases and the integral membrane protein EcfT) and an integral membrane protein responsible for substrate specificity (S-component). S-components for different substrates  may associate with the same energizing module. The energizing module from Lactococcus lactis has been shown to form stable complexes with each of the eight predicted S-components found in this organism. Using light scattering, EcfT, the two ATPases (EcfA and EcfA'), and the S-component were found to be present in a stoichiometric 1:1:1:1 ratio. The complexes were reconstituted in proteoliposomes and shown to mediate ATP-dependent transport. ECF-type transporters are the smallest known ABC transporters.

Energy coupling factor (ECF) transporters are a subgroup of ATP-binding cassette (ABC) transporters involved in the uptake of vitamins and micronutrients in prokaryotes. In contrast to classical ABC importers, ECF transporters do not make use of water-soluble substrate binding proteins or domains but instead employ integral membrane proteins for substrate binding (S-components or EcfS). S-components form active translocation complexes with the ECF module, an assembly of two nucleotide-binding domains (NBDs, or EcfA) and a second transmembrane 'energy transducer' protein, EcfT. In many cases, the ECF module can interact with several different S-components that bind diverse substrates. The modular organization with exchangeable S-components on a single ECF module allows the transport of chemically different substrates via a common route. The determination of the crystal structures of the S-components that recognize thiamin and riboflavin provided clues about the mechanism of S-component exchange. Erkens et al. (2012) described current views of the transport mechanism by ECF transporters.

Some ABC exporters act on protein substrates. Export depends on the ABC transporter, a periplasmic 'adapter', the membrane fusion proteins (MFPs; 8.A.1) and an outer membrane factor (OMF; 1.B.17). Assembly of the tripartite complex can be transient and induced upon binding of the substrate to the ABC protein. Masi & Wandersman (2010) showed that in addition to the C-terminal targeting sequence, many additional signals throughout the substrate protein facilitate secretion. Interaction of the C-terminal 'targeting' signal activates the ATPase activity, causing disassembly of the complex. Thus, the proposed 'targeting' motif may signal dissociation rather than targeting (Masi & Wandersman et al., 2010). Dassa and Bouige (2001) have devised a phylogenetic/functional classification system for ABC transporters that overlaps the TC system. In their system, several of the TC families are included in single families. These reveal the closer phylogenetic relationship of TC families as follows:

Jones & George (2012) reported molecular dynamics simulations of the ATP/apo and ATP/ADP states of the bacterial ABC exporter Sav1866 (TC#3.A.1.106.2). Conformers of the active site have a canonical geometry for an in-line nucleophilic attack on the ATP γ-phosphate. The conserved glutamate immediately downstream of the Walker B motif is the catalytic base, forming a dyad with the H-loop histidine, while the Q-loop glutamine has an organising role. Each D-loop provides a coordinating residue of the attacking water, and comparison with the simulation of the ATP/ADP state suggested that via their flexibility, the D-loops modulate formation of the hydrolysis-competent state. A global switch involving a coupling helix delineates the signal transmission route by which allosteric control of ATP hydrolysis in ABC transporters is mediated. 

Binding of ATP to the nucleotide binding domains (NBDs) of ABC proteins drives the dimerization of NBDs, which, in turn, causes large conformational changes within the transmembrane domains.  NBD dimerization proceeds with a large gain of water entropy when ATP molecules bind to the NBDs. The energetic gain arising from direct NBD-NBD interactions is canceled by the dehydration penalty and the configurational-entropy loss. ATP hydrolysis induces a loss of the shape complementarity between the NBDs, which leads to the dissociation of the dimer, due to a decrease in the water-entropy gain and an increase in the configurational-entropy loss (Hayashi et al. 2014).

ABC proteins play critical roles in maintaining lipid and sterol homeostasis in higher eukaryotes. In human, several subfamily-A and -G members function as cholesterol transporters across the cellular membranes. Deficiencies of these ABC proteins can cause dyslipidemia that is associated with health conditions such as atherosclerosis, diabetes, fatty liver disease, and neurodegeneration (Xavier et al. 2018). The physiological roles of ABC cholesterol transporters have been implicated in mediating cholesterol efflux for reverse cholesterol transport and in maintaining membrane integrity for cell survival.  The membrane constituents of ABC transporters may play key roles in determining the transport substrates and the translocation mechanisms via the transmembrane domains. High resolution structures of human sterol transporter ABCG5/G8 and its functional homologs have shed light on the structural features of ABC transporters. Xavier et al. 2018 outlined what is known about ABCG cholesterol transporters, addressed key structural features in the putative sterol translocation pathway on the transmembrane domains, and concluded by proposing a mechanistic model of ABC cholesterol transporters.

ABC peptide/protein exporters are usuallly believed to export their substrates directly from the cytoplasm to the extracellular medium without a periplasmic intermediate.  However, a subgroup of systems, linked with a bacterial transglutaminase-like cysteine proteinase (BTLCP) apparently uses a two-step secretion mechanism. BTLCP-linked T1SSs transport a class of repeats-in-toxin (RTX) adhesins that are critical for biofilm formation. The prototype of this RTX adhesin group, LapA of Pseudomonas fluorescens Pf0-1, uses a novel N-terminal retention module to anchor the adhesin at the cell surface as a secretion intermediate threaded through the outer membrane-localized TolC-like protein LapE. This secretion intermediate is posttranslationally cleaved by the BTLCP family LapG protein to release LapA from its cognate T1SS pore. Thus, the secretion of LapA and related RTX adhesins into the extracellular environment appears to be a T1SS-mediated two-step process that involves a periplasmic intermediate (Smith et al. 2018).

The ABC-F family comprises an extremely diverse set of cytoplasmic ATPase proteins. All of the proteins in the ABC-F family characterized act on the ribosome and are translation factors (Ousalem et al. 2019). Their common function is ATP-dependent modulation of the stereochemistry of the peptidyl transferase center (PTC) in the ribosome coupled to changes in its global conformation and P-site tRNA binding geometry. Ousalem et al. 2019 presented an overview of the function, structure, and theories for the mechanisms-of-action of microbial ABC-F proteins including those involved in mediating resistance to ribosome-binding antibiotics.

Xiao et al. 2022 identified 87 ABC transporter genes in the genomes of Tenebrio molitor as well as those from Asbolus verrucosus (104), Hycleus cichorii (65), and Hycleus phaleratus (80). Combining these genes (336 in total) with published genes reported for Tribolium castaneum, the phylogeny of ABC transporter genes in all five Tenebrionids were analyzed. They were assigned to eight subfamilies (ABCA-H). In comparison to other species, the ABCC subfamily in this group of beetles appears expanded. The expression profiles of the T. molitor genes at different life stages and in various tissues were also investigated using transcriptomic analysis. Most of them display developmental specific expression patterns, suggesting their possible roles in development. Most of them are highly expressed in detoxification-related tissues including the gut and Malpighian tubule, from which roles in insecticide resistance were suggested. We detected specific or abundant expression of many ABC transporter genes in various tissues such as salivary gland, ovary, testis, and antenna (Xiao et al. 2022).

Dassa and Bouige (2001) summarized the protein and domain organization of each of the various family-type proteins (see Table 1). Based on the structures, a general mechanism for ABC transporters has been proposed, known as the Switch or Alternating Access Model, which holds that the NBDs are widely separated, with the TMDs and NBDs together forming an intracellular-facing inverted 'V' shape. Binding of two ATPs and the substrate to the inward-facing conformation induces a transition to an outward conformation. Despite this apparent progress, certainty around the transport mechanism for any given ABC remains elusive (Jones and George 2023). How substrate binding and transport is coupled to ATP binding and hydrolysis is not known, and there is a large body of biochemical and biophysical data that is at odds with widely separated NBDs being a functional/physiological state. An alternative Constant Contact model has been proposed in which the two NBSs operate 180 degrees out of phase with respect to ATP hydrolysis, with the NBDs remaining in close proximity throughout the transport cycle and operating in an asymmetric allosteric manner (Jones and George 2023).


Table 1
D&B Family TC Families
MOI SulT, + PhoT + MolT + FeT + POPT + ThiT
OTCN QAT + NitT + TauT
DPL Lipid E + Glucan E + Prot1E + Prot2E + Pep1E + Pep2E + Pep3E + DrugE2 + DrugE3 + MDR + CFTR + Ste + TAP + HMT + MPE
DRA DrugE1 + CPR

The generalized transport reaction for ABC-type uptake systems is:

Solute (out) + ATP → Solute (in) + ADP + Pi.

The generalized transport reaction for ABC-type efflux systems is:

Substrate (in) + ATP → Substrate (out) + ADP + Pi.

This family belongs to the: ArsA ATPase (ArsA) Superfamily.

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