Abstract
ATP-binding cassette (ABC) transporters are one of the largest families of membrane proteins in prokaryotic organisms. Much is now understood about the structure of these transporters and many reviews have been written on that subject. In contrast, less has been written on the assembly of ABC transporter complexes and this will be a major focus of this book chapter. The complexes are formed from two cytoplasmic subunits that are highly conserved (in terms of their primary and three-dimensional structures) across the whole family. These ATP-binding subunits give rise to the name of the family. They must assemble with two transmembrane subunits that will typically form the permease component of the transporter. The transmembrane subunits have been found to be surprisingly diverse in structure when the whole family is examined, with seven distinct folds identified so far. Hence nucleotide-binding subunits appear to have been bolted on to a variety of transmembrane platforms during evolution, leading to a greater variety in function. Furthermore, many importers within the family utilise a further external substrate-binding component to trap scarce substrates and deliver them to the correct permease components. In this chapter, we will discuss whether assembly of the various ABC transporter subunits occurs with high fidelity within the crowded cellular environment and whether promiscuity in assembly of transmembrane and cytoplasmic components can occur. We also discuss the new AlphaFold protein structure prediction tool which predicts a new type of transmembrane domain fold within the ABC transporters that is associated with cation exporters of bacteria and plants.
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References
Adams MD, Wagner LM, Graddis TJ, Landick R, Antonucci TK, Gibson AL, Oxender DL (1990) Nucleotide sequence and genetic characterization reveal six essential genes for the LIV-I and LS transport systems of Escherichia coli. J Biol Chem 265(20):11436–11443
Aiba H, Baba T, Hayashi K, Inada T, Isono K, Itoh T, Kasai H, Kashimoto K, Kimura S, Kitakawa M, Kitagawa M, Makino K, Miki T, Mizobuchi K, Mori H, Mori T, Motomura K, Nakade S, Nakamura Y, Nashimoto H, Nishio Y, Oshima T, Saito N, Sampei G, Horiuchi T et al (1996) A 570-kb DNA sequence of the Escherichia coli K-12 genome corresponding to the 28.0-40.1 min region on the linkage map. DNA Res 3(6):363–377. https://doi.org/10.1093/dnares/3.6.363
Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, Harrell PM, Trinh YT, Zhang Q, Urbatsch IL, Chang G (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323(5922):1718–1722
Altschul SF, Koonin EV (1998) Iterated profile searches with PSI-BLAST--a tool for discovery in protein databases. Trends Biochem Sci 23(11):444–447. https://doi.org/10.1016/s0968-0004(98)01298-5
Babu M, Bundalovic-Torma C, Calmettes C, Phanse S, Zhang Q, Jiang Y, Minic Z, Kim S, Mehla J, Gagarinova A, Rodionova I, Kumar A, Guo H, Kagan O, Pogoutse O, Aoki H, Deineko V, Caufield JH, Holtzapple E, Zhang Z, Vastermark A, Pandya Y, Lai CC, El Bakkouri M, Hooda Y, Shah M, Burnside D, Hooshyar M, Vlasblom J, Rajagopala SV, Golshani A, Wuchty S, Greenblatt JF, Saier M, Uetz P, Moraes TF, Parkinson J, Emili A (2018) Global landscape of cell envelope protein complexes in Escherichia coli. Nat Biotechnol 36(1):103–112. https://doi.org/10.1038/nbt.4024
Ban N, Freeborn B, Nissen P, Penczek P, Grassucci RA, Sweet R, Frank J, Moore PB, Steitz TA (1998) A 9 A resolution X-ray crystallographic map of the large ribosomal subunit. Cell 93(7):1105–1115. https://doi.org/10.1016/s0092-8674(00)81455-5
Ban N, Nissen P, Hansen J, Moore PB, Steitz TA (2000) The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289(5481):905–920. https://doi.org/10.1126/science.289.5481.905
Bardin S, Dan S, Osteras M, Finan TM (1996) A phosphate transport system is required for symbiotic nitrogen fixation by Rhizobium meliloti. J Bacteriol 178(15):4540–4547. https://doi.org/10.1128/jb.178.15.4540-4547.1996
Bell AW, Buckel SD, Groarke JM, Hope JN, Kingsley DH, Hermodson MA (1986) The nucleotide sequences of the rbsD, rbsA, and rbsC genes of Escherichia coli K12. J Biol Chem 261(17):7652–7658
Berntsson RP-A, ter Beek J, Majsnerowska M, Duurkens RH, Puri P, Poolman B, Slotboom D-J (2012) Structural divergence of paralogous S components from ECF-type ABC transporters. Proc Natl Acad Sci U S A 109(35):13990–13995
Bertolini M, Fenzl K, Kats I, Wruck F, Tippmann F, Schmitt J, Auburger JJ, Tans S, Bukau B, Kramer G (2021) Interactions between nascent proteins translated by adjacent ribosomes drive homomer assembly. Science 371(6524):57–64. https://doi.org/10.1126/science.abc7151
Bi Y, Mann E, Whitfield C, Zimmer J (2018) Architecture of a channel-forming O-antigen polysaccharide ABC transporter. Nature 553(7688):361–365. https://doi.org/10.1038/nature25190
Borths EL, Poolman B, Hvorup RN, Locher KP, Rees DC (2005) In vitro functional characterization of BtuCD-F, the Escherichia coli ABC transporter for vitamin B12 uptake. Biochemistry 44(49):16301–16309. https://doi.org/10.1021/bi0513103
Braibant M, Lefèvre P, de Wit L, Peirs P, Ooms J, Huygen K, Andersen AB, Content J (1996) A Mycobacterium tuberculosis gene cluster encoding proteins of a phosphate transporter homologous to the Escherichia coli Pst system. Gene 176(1–2):171–176. https://doi.org/10.1016/0378-1119(96)00242-9
Bruntner C, Lauer B, Schwarz W, Möhrle V, Bormann C (1999) Molecular characterization of co-transcribed genes from Streptomyces tendae Tü901 involved in the biosynthesis of the peptidyl moiety of the peptidyl nucleoside antibiotic nikkomycin. Mol Gen Genet 262(1):102–114. https://doi.org/10.1007/pl00008637
Caffalette CA, Corey RA, Sansom MSP, Stansfeld PJ, Zimmer J (2019) A lipid gating mechanism for the channel-forming O antigen ABC transporter. Nat Commun 10(1):824. https://doi.org/10.1038/s41467-019-08646-8
Callaghan R, Ford RC, Kerr ID (2006) The translocation mechanism of P-glycoprotein. FEBS Lett 580(4):1056–1063. https://doi.org/10.1016/j.febslet.2005.11.083
Chai C, Yu Y, Zhuo W, Zhao H, Li X, Wang N, Chai J, Yang M (2013) Structural basis for a homodimeric ATPase subunit of an ECF transporter. Protein Cell 4(10):793–801
Chandravanshi M, Gogoi P, Kanaujia SP (2016) Computational characterization of TTHA0379: A potential glycerophosphocholine binding protein of Ugp ATP-binding cassette transporter. Gene 592(2):260–268. https://doi.org/10.1016/j.gene.2016.07.017
Checroun C, Gutierrez C (2004) Sigma(s)-dependent regulation of yehZYXW, which encodes a putative osmoprotectant ABC transporter of Escherichia coli. FEMS Microbiol Lett 236(2):221–226. https://doi.org/10.1016/j.femsle.2004.05.046
Chen B, Boel G, Hashem Y, Ning W, Fei J, Wang C, Gonzalez RL Jr, Hunt JF, Frank J (2014) EttA regulates translation by binding the ribosomal E site and restricting ribosome-tRNA dynamics. Nat Struct Mol Biol 21(2):152–159. https://doi.org/10.1038/nsmb.2741
Chen L, Hou WT, Fan T, Liu B, Pan T, Li YH, Jiang YL, Wen W, Chen ZP, Sun L, Zhou CZ, Chen Y (2020) Cryo-electron microscopy structure and transport mechanism of a wall teichoic acid ABC transporter. mBio 11(2):e02749-19. https://doi.org/10.1128/mBio.02749-19
Chenault SS, Earhart CF (1992) Identification of hydrophobic proteins FepD and FepG of the Escherichia coli ferrienterobactin permease. Microbiology 138(10):2167–2171. https://doi.org/10.1099/00221287-138-10-2167
Chin N, Frey J, Chang CF, Chang YF (1996) Identification of a locus involved in the utilization of iron by Actinobacillus pleuropneumoniae. FEMS Microbiol Lett 143(1):1–6. https://doi.org/10.1111/j.1574-6968.1996.tb08452.x
Chng SS, Gronenberg LS, Kahne D (2010) Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry 49(22):4565–4567. https://doi.org/10.1021/bi100493e
Choi CC, Ford RC (2021) ATP binding cassette importers in eukaryotic organisms. Biol Rev Camb Philos Soc 96:1318–1330. https://doi.org/10.1111/brv.12702
Choudhury HG, Tong Z, Mathavan I, Li Y, Iwata S, Zirah S, Rebuffat S, Van Veen HW, Beis K (2014) Structure of an antibacterial peptide ATP-binding cassette transporter in a novel outward occluded state. Proc Natl Acad Sci U S A 111(25):9145–9150
Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, Deeley RG (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258(5088):1650–1654
Corbalan N, Runti G, Adler C, Covaceuszach S, Ford RC, Lamba D, Beis K, Scocchi M, Vincent PA (2013) Functional and structural study of the dimeric inner membrane protein SbmA. J Bacteriol 195(23):5352–5361. https://doi.org/10.1128/JB.00824-13
Crow A, Greene NP, Kaplan E, Koronakis V (2017) Structure and mechanotransmission mechanism of the MacB ABC transporter superfamily. Proc Natl Acad Sci U S A 114(47):12572–12577. https://doi.org/10.1073/pnas.1712153114
Cruz-Ramos H, Cook G, Wu G, Cleeter M, Poole R (2004) Membrane topology and mutational analysis of Escherichia coli CydDC, an ABC-type cysteine exporter required for cytochrome assembly. Microbiology 150:3415–3427. https://doi.org/10.1099/mic.0.27191-0
Daley DO, Rapp M, Granseth E, Melén K, Drew D, Von Heijne G (2005) Global topology analysis of the Escherichia coli inner membrane proteome. Science 308(5726):1321–1323
Davis JJ, Wattam AR, Aziz RK, Brettin T, Butler R, Butler RM, Chlenski P, Conrad N, Dickerman A, Dietrich EM, Gabbard JL, Gerdes S, Guard A, Kenyon RW, Machi D, Mao C, Murphy-Olson D, Nguyen M, Nordberg EK, Olsen GJ, Olson RD, Overbeek JC, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomas C, VanOeffelen M, Vonstein V, Warren AS, Xia F, Xie D, Yoo H, Stevens R (2020) The PATRIC Bioinformatics Resource Center: expanding data and analysis capabilities. Nucleic Acids Res 48(D1):D606–D612. https://doi.org/10.1093/nar/gkz943
Dawson RJ, Locher KP (2006) Structure of a bacterial multidrug ABC transporter. Nature 443(7108):180–185
Dawson RJ, Locher KP (2007) Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett 581(5):935–938
de Leeuw E, Graham B, Phillips GJ, ten Hagen-Jongman CM, Oudega B, Luirink J (1999) Molecular characterization of Escherichia coli FtsE and FtsX. Mol Microbiol 31(3):983–993. https://doi.org/10.1046/j.1365-2958.1999.01245.x
Dean M, Allikmets R (2001) Complete characterization of the human ABC gene family. J Bioenerg Biomembr 33(6):475–479
Dean M, Annilo T (2005) Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 6:123–142. https://doi.org/10.1146/annurev.genom.6.080604.162122
Dean M, Rzhetsky A, Allikmets R (2001) The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11(7):1156–1166. https://doi.org/10.1101/gr.184901
Di Bartolo ND, Hvorup RN, Locher KP, Booth PJ (2011) In vitro folding and assembly of the Escherichia coli ATP-binding cassette transporter, BtuCD. J Biol Chem 286(21):18807–18815. https://doi.org/10.1074/jbc.M110.176891
Dohme F, Nierhaus KH (1976) Total reconstitution and assembly of 50 S subunits from Escherichia coli Ribosomes in vitro. J Mol Biol 107(4):585–599. https://doi.org/10.1016/s0022-2836(76)80085-x
Duncan CD, Mata J (2011) Widespread cotranslational formation of protein complexes. PLoS Genet 7(12):e1002398. https://doi.org/10.1371/journal.pgen.1002398
Eckey V, Landmesser H, Schneider E (2010) Studying subunit-subunit interactions in a bacterial ABC transporterby in vitro assembly. Biochim Biophys Acta 1798(6):1250–1253. https://doi.org/10.1016/j.bbamem.2010.03.001
Eitinger T, Rodionov DA, Grote M, Schneider E (2011) Canonical and ECF-type ATP-binding cassette importers in prokaryotes: diversity in modular organization and cellular functions. FEMS Microbiol Rev 35(1):3–67
Elferink RPO, Paulusma CC (2007) Function and pathophysiological importance of ABCB4 (MDR3 P-glycoprotein). Pflügers Arch Eur J Physiol 453(5):601–610
Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2(4):953–971. https://doi.org/10.1038/nprot.2007.131
Erkens GB, Berntsson RP, Fulyani F, Majsnerowska M, Vujičić-Žagar A, Ter Beek J, Poolman B, Slotboom DJ (2011) The structural basis of modularity in ECF-type ABC transporters. Nat Struct Mol Biol 18(7):755–760
Erkens GB, Majsnerowska M, ter Beek J, Slotboom DJ (2012) Energy coupling factor-type ABC transporters for vitamin uptake in prokaryotes. Biochemistry 51(22):4390–4396
Fabre L, Bao H, Innes J, Duong F, Rouiller I (2017) Negative stain single-particle EM of the maltose transporter in nanodiscs reveals asymmetric closure of MalK(2) and catalytic roles of ATP, MalE, and Maltose. J Biol Chem 292(13):5457–5464. https://doi.org/10.1074/jbc.M116.757898
Feng Y, Chen CS, Ho J, Pearce D, Hu S, Wang B, Desai P, Kim KS, Zhu H (2018) High-throughput chip assay for investigating Escherichia coli interaction with the blood-brain barrier using microbial and human proteome microarrays (dual-microarray technology). Anal Chem 90(18):10958–10966. https://doi.org/10.1021/acs.analchem.8b02513
Ferreira MJ, Sá-Nogueira I (2010) A multitask ATPase serving different ABC-type sugar importers in Bacillus subtilis. J Bacteriol 192(20):5312–5318
Ferreira MJ, Mendes AL, de Sa-Nogueira I (2017) The MsmX ATPase plays a crucial role in pectin mobilization by Bacillus subtilis. PLoS One 12(12):e0189483
Finkenwirth F, Neubauer O, Gunzenhäuser J, Schoknecht J, Scolari S, Stöckl M, Korte T, Herrmann A, Eitinger T (2010) Subunit composition of an energy-coupling-factor-type biotin transporter analysed in living bacteria. Biochem J 431(3):373–381
Finkenwirth F, Sippach M, Landmesser H, Kirsch F, Ogienko A, Grunzel M, Kiesler C, Steinhoff H-J, Schneider E, Eitinger T (2015) ATP-dependent conformational changes trigger substrate capture and release by an ECF-type biotin transporter. J Biol Chem 290(27):16929–16942
Fisher DJ, Fernández RE, Adams NE, Maurelli AT (2012) Uptake of biotin by Chlamydia spp. through the use of a bacterial transporter (BioY) and a host-cell transporter (SMVT)
Fitzpatrick AWP, Llabres S, Neuberger A, Blaza JN, Bai XC, Okada U, Murakami S, van Veen HW, Zachariae U, Scheres SHW, Luisi BF, Du D (2017) Structure of the MacAB-TolC ABC-type tripartite multidrug efflux pump. Nat Microbiol 2:17070. https://doi.org/10.1038/nmicrobiol.2017.70
Ford RC, Beis K (2019) Learning the ABCs one at a time: structure and mechanism of ABC transporters. Biochem Soc Trans 47(1):23–36. https://doi.org/10.1042/BST20180147
Ford RC, Hellmich UA (2020) What monomeric nucleotide binding domains can teach us about dimeric ABC proteins. FEBS Lett 594(23):3857–3875. https://doi.org/10.1002/1873-3468.13921
Ford RC, Marshall-Sabey D, Schuetz J (2020) Linker domains: why ABC transporters ‘live in fragments no longer’. Trends Biochem Sci 45(2):137–148. https://doi.org/10.1016/j.tibs.2019.11.004
Freinkman E, Okuda S, Ruiz N, Kahne D (2012) Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export. Biochemistry 51(24):4800–4806. https://doi.org/10.1021/bi300592c
French JB, Zhao H, An S, Niessen S, Deng Y, Cravatt BF, Benkovic SJ (2013) Hsp70/Hsp90 chaperone machinery is involved in the assembly of the purinosome. Proc Natl Acad Sci U S A 110(7):2528–2533. https://doi.org/10.1073/pnas.1300173110
Ghilarov D, Inaba-Inoue S, Stepien P, Qu F, Michalczyk E, Pakosz Z, Nomura N, Ogasawara S, Walker GC, Rebuffat S, Iwata S, Heddle JG, Beis K (2021) Molecular mechanism of SbmA, a promiscuous transporter exploited by antimicrobial peptides. Sci Adv 7(37):eabj5363. https://doi.org/10.1126/sciadv.abj5363
Gopal S, Berg D, Hagen N, Schriefer E-M, Stoll R, Goebel W, Kreft J (2010) Maltose and maltodextrin utilization by Listeria monocytogenes depend on an inducible ABC transporter which is repressed by glucose. PLoS One 5(4):e10349
Gopinath K, Venclovas Č, Ioerger TR, Sacchettini JC, McKinney JD, Mizrahi V, Warner DF (2013) A vitamin B12 transporter in Mycobacterium tuberculosis. Open Biol 3(2):120175
Gradhand U, Kim RB (2008) Pharmacogenomics of MRP Transporters (ABCC1-5) and BCRP (ABCG2). Drug Metab Rev 40(2):317–354
Haardt M, Bremer E (1996) Use of phoA and lacZ fusions to study the membrane topology of ProW, a component of the osmoregulated ProU transport system of Escherichia coli. J Bacteriol 178:5370–5381. https://doi.org/10.1128/jb.178.18.5370-5381.1996
Halbach A, Zhang H, Wengi A, Jablonska Z, Gruber IML, Halbeisen RE, Dehé P-M, Kemmeren P, Holstege F, Géli V, Gerber AP, Dichtl B (2009) Cotranslational assembly of the yeast SET1C histone methyltransferase complex. EMBO J 28(19):2959–2970
Hebbeln P, Rodionov DA, Alfandega A, Eitinger T (2007) Biotin uptake in prokaryotes by solute transporters with an optional ATP-binding cassette-containing module. Proc Natl Acad Sci U S A 104(8):2909–2914
Henderson GB, Zevely EM, Huennekens F (1979) Mechanism of folate transport in Lactobacillus casei: evidence for a component shared with the thiamine and biotin transport systems. J Bacteriol 137(3):1308–1314
Herold M, Nierhaus KH (1987) Incorporation of six additional proteins to complete the assembly map of the 50 S subunit from Escherichia coli ribosomes. J Biol Chem 262(18):8826–8833
Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113
Higgins CF, Ames GF (1981) Two periplasmic transport proteins which interact with a common membrane receptor show extensive homology: complete nucleotide sequences. Proc Natl Acad Sci U S A 78(10):6038–6042. https://doi.org/10.1073/pnas.78.10.6038
Higgins CF, Ames GF (1982) Regulatory regions of two transport operons under nitrogen control: nucleotide sequences. Proc Natl Acad Sci U S A 79(4):1083–1087. https://doi.org/10.1073/pnas.79.4.1083
Higgins CF, Haag PD, Nikaido K, Ardeshir F, Garcia G, Ames GF (1982) Complete nucleotide sequence and identification of membrane components of the histidine transport operon of S. typhimurium. Nature 298(5876):723–727
Hohl M, Briand C, Grütter MG, Seeger MA (2012) Crystal structure of a heterodimeric ABC transporter in its inward-facing conformation. Nat Struct Mol Biol 19(4):395–402
Hollenstein K, Frei DC, Locher KP (2007) Structure of an ABC transporter in complex with its binding protein. Nature 446(7132):213–216
Horler RS, Müller A, Williamson DC, Potts JR, Wilson KS, Thomas GH (2009) Furanose-specific sugar transport: characterization of a bacterial galactofuranose-binding protein. J Biol Chem 284(45):31156–31163. https://doi.org/10.1074/jbc.M109.054296
Hsu WL, Furuta T, Sakurai M (2018) The mechanism of nucleotide-binding domain dimerization in the intact maltose transporter as studied by all-atom molecular dynamics simulations. Proteins 86(2):237–247. https://doi.org/10.1002/prot.25433
Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21(2):655–667. https://doi.org/10.1105/tpc.108.064543
Hurtubise Y, Shareck F, Kluepfel D, Morosoli R (1995) A cellulase/xylanase-negative mutant of Streptomyces lividans 1326 defective in cellobiose and xylobiose uptake is mutated in a gene encoding a protein homologous to ATP-binding proteins. Mol Microbiol 17(2):367–377
Ito Y, Matsuzawa H, Matsuyama S, Narita S, Tokuda H (2006) Genetic analysis of the mode of interplay between an ATPase subunit and membrane subunits of the lipoprotein-releasing ATP-binding cassette transporter LolCDE. J Bacteriol 188(8):2856–2864. https://doi.org/10.1128/JB.188.8.2856-2864.2006
Jardetzky O (1966) Simple allosteric model for membrane pumps. Nature 211(5052):969–970. https://doi.org/10.1038/211969a0
Joglekar AP, Hay JC (2005) Evidence for regulation of ER/Golgi SNARE complex formation by hsc70 chaperones. Eur J Cell Biol 84(5):529–542. https://doi.org/10.1016/j.ejcb.2004.12.028
Jones MM, Johnson A, Koszelak-Rosenblum M, Kirkham C, Brauer AL, Malkowski MG, Murphy TF (2014) Role of the oligopeptide permease ABC Transporter of Moraxella catarrhalis in nutrient acquisition and persistence in the respiratory tract. Infect Immun 82(11):4758–4766. https://doi.org/10.1128/iai.02185-14
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Zidek A, Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J, Back T, Petersen S, Reiman D, Clancy E, Zielinski M, Steinegger M, Pacholska M, Berghammer T, Bodenstein S, Silver D, Vinyals O, Senior AW, Kavukcuoglu K, Kohli P, Hassabis D (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596(7873):583–589. https://doi.org/10.1038/s41586-021-03819-2
Kana BD, Weinstein EA, Avarbock D, Dawes SS, Rubin H, Mizrahi V (2001) Characterization of the cydAB-encoded cytochrome bd oxidase from Mycobacterium smegmatis. J Bacteriol 183(24):7076–7086. https://doi.org/10.1128/JB.183.24.7076-7086.2001
Kanamaru K, Taniguchi N, Miyamoto S, Narita S, Tokuda H (2007) Complete reconstitution of an ATP-binding cassette transporter LolCDE complex from separately isolated subunits. FEBS J 274(12):3034–3043. https://doi.org/10.1111/j.1742-4658.2007.05832.x
Karpowich NK, Wang D-N (2013) Assembly and mechanism of a group II ECF transporter. Proc Natl Acad Sci 110(7):2534–2539
Kashiwayama Y, Seki M, Yasui A, Murasaki Y, Morita M, Yamashita Y, Sakaguchi M, Tanaka Y, Imanaka T (2009) 70-kDa peroxisomal membrane protein related protein (P70R/ABCD4) localizes to endoplasmic reticulum not peroxisomes, and NH2-terminal hydrophobic property determines the subcellular localization of ABC subfamily D proteins. Exp Cell Res 315(2):190–205
Kerppola RE, Ames GF (1992) Topology of the hydrophobic membrane-bound components of the histidine periplasmic permease. Comparison with other members of the family. J Biol Chem 267(4):2329–2336
Kerppola RE, Shyamala VK, Klebba P, Ames GF (1991) The membrane-bound proteins of periplasmic permeases form a complex. Identification of the histidine permease HisQMP complex. J Biol Chem 266(15):9857–9865
Kertesz MA (2001) Bacterial transporters for sulfate and organosulfur compounds. Res Microbiol 152(3–4):279–290. https://doi.org/10.1016/s0923-2508(01)01199-8
Keseler IM, Mackie A, Peralta-Gil M, Santos-Zavaleta A, Gama-Castro S, Bonavides-Martínez C, Fulcher C, Huerta AM, Kothari A, Krummenacker M, Latendresse M, Muñiz-Rascado L, Ong Q, Paley S, Schröder I, Shearer AG, Subhraveti P, Travers M, Weerasinghe D, Weiss V, Collado-Vides J, Gunsalus RP, Paulsen I, Karp PD (2013) EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res 41(Database issue):D605–D612. https://doi.org/10.1093/nar/gks1027
Koch DJ, Rückert C, Rey DA, Mix A, Pühler A, Kalinowski J (2005) Role of the ssu and seu genes of Corynebacterium glutamicum ATCC 13032 in utilization of sulfonates and sulfonate esters as sulfur sources. Appl Environ Microbiol 71(10):6104–6114. https://doi.org/10.1128/aem.71.10.6104-6114.2005
Kos V, Ford RC (2009) The ATP-binding cassette family: a structural perspective. Cell Mol Life Sci 66(19):3111–3126. https://doi.org/10.1007/s00018-009-0064-9
Köster W, Böhm B (1992) Point mutations in two conserved glycine residues within the integral membrane protein FhuB affect iron(II) hydroxamate transport. Mol Gen Genet MGG 232(3):399–407. https://doi.org/10.1007/BF00266243
Kramer G, Shiber A, Bukau B (2019) Mechanisms of cotranslational maturation of newly synthesized proteins. Annu Rev Biochem 88:337–364. https://doi.org/10.1146/annurev-biochem-013118-111717
Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372(3):774–797. https://doi.org/10.1016/j.jmb.2007.05.022
Lebrette H, Brochier-Armanet C, Zambelli B, de Reuse H, Borezée-Durant E, Ciurli S, Cavazza C (2014) Promiscuous nickel import in human pathogens: structure, thermodynamics, and evolution of extracytoplasmic nickel-binding proteins. Structure 22(10):1421–1432
Lee JY, Yang JG, Zhitnitsky D, Lewinson O, Rees DC (2014) Structural characterization of heavy metal detoxification by a bacterial Atm1-family ABC transporter
Lee JY, Kinch LN, Borek DM, Wang J, Wang J, Urbatsch IL, Xie XS, Grishin NV, Cohen JC, Otwinowski Z, Hobbs HH, Rosenbaum DM (2016) Crystal structure of the human sterol transporter ABCG5/ABCG8. Nature 533(7604):561–564. https://doi.org/10.1038/nature17666
Lehman T, Mallireddy V, Seddon M, Modali R, Ratnasinghe L (2008) Association between an ABCC8/SUR1 polymorphism and breast cancer risk. AACR
Leisico F, Godinho LM, Goncalves IC, Silva SP, Carneiro B, Romao MJ, Santos-Silva T, de Sa-Nogueira I (2020) Multitask ATPases (NBDs) of bacterial ABC importers type I and their interspecies exchangeability. Sci Rep 10(1):19564. https://doi.org/10.1038/s41598-020-76444-0
Lennen R (2007) Inhibitors of autoinducer-2 quorum sensing and their effect on bacterial biofilm formation
Leonard BA, Podbielski A, Hedberg PJ, Dunny GM (1996) Enterococcus faecalis pheromone binding protein, PrgZ, recruits a chromosomal oligopeptide permease system to import sex pheromone cCF10 for induction of conjugation. Proc Natl Acad Sci U S A 93(1):260–264. https://doi.org/10.1073/pnas.93.1.260
Li Y, Orlando BJ, Liao M (2019) Structural basis of lipopolysaccharide extraction by the LptB2FGC complex. Nature 567(7749):486–490. https://doi.org/10.1038/s41586-019-1025-6
Lin DY, Huang S, Chen J (2015) Crystal structures of a polypeptide processing and secretion transporter. Nature 523(7561):425–430. https://doi.org/10.1038/nature14623
Linke CM, Woodiga SA, Meyers DJ, Buckwalter CM, Salhi HE, King SJ (2013) The ABC transporter encoded at the pneumococcal fructooligosaccharide utilization locus determines the ability to utilize long-and short-chain fructooligosaccharides. J Bacteriol 195(5):1031–1041
Linton KJ, Higgins CF (1998) The Escherichia coli ATP-binding cassette (ABC) proteins. Mol Microbiol 28(1):5–13
Liu PQ, Ames GF (1998) In vitro disassembly and reassembly of an ABC transporter, the histidine permease. Proc Natl Acad Sci U S A 95(7):3495–3500. https://doi.org/10.1073/pnas.95.7.3495
Liu F, Jones DK, de Lange WJ, Robertson GA (2016) Cotranslational association of mRNA encoding subunits of heteromeric ion channels. Proc Natl Acad Sci U S A 113(17):4859–4864. https://doi.org/10.1073/pnas.1521577113
Liu J, Hou LL, Zhao CY (2018) Effect of YHHJ on the expression of the hepatocellular bile acid transporters multidrug resistance-associated protein 2 and bile salt export pump in ethinylestradiol-induced cholestasis. Exp Ther Med 15(4):3699–3704. https://doi.org/10.3892/etm.2018.5891
Locher KP, Lee AT, Rees DC (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296(5570):1091–1098
Luo Q, Yang X, Yu S, Shi H, Wang K, Xiao L, Zhu G, Sun C, Li T, Li D, Zhang X, Zhou M, Huang Y (2017) Structural basis for lipopolysaccharide extraction by ABC transporter LptB2FG. Nat Struct Mol Biol 24(5):469–474. https://doi.org/10.1038/nsmb.3399
Majsnerowska M, Ter Beek J, Stanek WK, Duurkens RH, Slotboom DJ (2015) Competition between different S-components for the shared energy coupling factor module in energy coupling factor transporters. Biochemistry 54(31):4763–4766. https://doi.org/10.1021/acs.biochem.5b00609
Makhnevych T, Houry WA (2012) The role of Hsp90 in protein complex assembly. Biochim Biophys Acta 1823(3):674–682. https://doi.org/10.1016/j.bbamcr.2011.09.001
Malinverni J, Silhavy T (2009) An ABC transport system that maintains lipid asymmetry in the Gram-negative outer membrane. Proc Natl Acad Sci U S A 106:8009–8014. https://doi.org/10.1073/pnas.0903229106
Marion C, Aten AE, Woodiga SA, King SJ (2011) Identification of an ATPase, MsmK, which energizes multiple carbohydrate ABC transporters in Streptococcus pneumoniae. Infect Immun 79(10):4193–4200
Matthysse AG, Yarnall HA, Young N (1996) Requirement for genes with homology to ABC transport systems for attachment and virulence of Agrobacterium tumefaciens. J Bacteriol 178(17):5302–5308. https://doi.org/10.1128/jb.178.17.5302-5308.1996
Merlin C, Gardiner G, Durand S, Masters M (2002) The Escherichia coli metD locus encodes an ABC transporter which includes Abc (MetN), YaeE (MetI), and YaeC (MetQ). J Bacteriol 184(19):5513–5517. https://doi.org/10.1128/JB.184.19.5513-5517.2002
Morabbi Heravi K, Watzlawick H, Altenbuchner J (2019) The melREDCA operon encodes a utilization system for the raffinose family of oligosaccharides in Bacillus subtilis. J Bacteriol 201(15):e00109–e00119
Morgan JLW, Acheson JF, Zimmer J (2017) Structure of a type-1 secretion system ABC transporter. Structure 25(3):522–529. https://doi.org/10.1016/j.str.2017.01.010
Moussatova A, Kandt C, O'Mara ML, Tieleman DP (2008) ATP-binding cassette transporters in Escherichia coli. Biochim Biophys Acta Biomembr 1778(9):1757–1771. https://doi.org/10.1016/j.bbamem.2008.06.009
Mukherjee K, Huddleston JP, Narindoshvili T, Nemmara VV, Raushel FM (2019) Functional characterization of the ycjQRS gene cluster from Escherichia coli: a novel pathway for the transformation of d-gulosides to d-glucosides. Biochemistry 58(10):1388–1399. https://doi.org/10.1021/acs.biochem.8b01278
Narita S, Tanaka K, Matsuyama S, Tokuda H (2002) Disruption of lolCDE, encoding an ATP-binding cassette transporter, is lethal for Escherichia coli and prevents release of lipoproteins from the inner membrane. J Bacteriol 184(5):1417–1422. https://doi.org/10.1128/jb.184.5.1417-1422.2002
Netzer WJ, Hartl FU (1998) Protein folding in the cytosol: chaperonin-dependent and -independent mechanisms. Trends Biochem Sci 23(2):68–73. https://doi.org/10.1016/s0968-0004(97)01171-7
Neubauer H, Pantel I, Lindgren PE, Götz F (1999) Characterization of the molybdate transport system ModABC of Staphylococcus carnosus. Arch Microbiol 172(2):109–115. https://doi.org/10.1007/s002030050747
Neubauer O, Alfandega A, Schoknecht J, Sternberg U, Pohlmann A, Eitinger T (2009) Two essential arginine residues in the T components of energy-coupling factor transporters. J Bacteriol 191(21):6482–6488
Neubauer O, Reiffler C, Behrendt L, Eitinger T (2011) Interactions among the A and T units of an ECF-type biotin transporter analyzed by site-specific crosslinking. PLoS One 6(12):e29087
Nicolaou SA, Fast AG, Nakamaru-Ogiso E, Papoutsakis ET (2013) Overexpression of fetA (ybbL) and fetB (ybbM), encoding an iron exporter, enhances resistance to oxidative stress in Escherichia coli. Appl Environ Microbiol 79(23):7210–7219. https://doi.org/10.1128/AEM.02322-13
Nissen P, Hansen J, Ban N, Moore PB, Steitz TA (2000) The structural basis of ribosome activity in peptide bond synthesis. Science 289(5481):920–930. https://doi.org/10.1126/science.289.5481.920
Nöll A, Thomas C, Herbring V, Zollmann T, Barth K, Mehdipour AR, Tomasiak TM, Brüchert S, Joseph B, Abele R (2017) Crystal structure and mechanistic basis of a functional homolog of the antigen transporter TAP. Proc Natl Acad Sci U S A 114(4):E438–E447
Nomura M (1973) Assembly of bacterial ribosomes. Science 179(4076):864–873. https://doi.org/10.1126/science.179.4076.864
Okada U, Yamashita E, Neuberger A, Morimoto M, van Veen HW, Murakami S (2017) Crystal structure of tripartite-type ABC transporter MacB from Acinetobacter baumannii. Nat Commun 8(1):1336. https://doi.org/10.1038/s41467-017-01399-2
Okamoto S, Eltis LD (2011) The biological occurrence and trafficking of cobalt. Metallomics 3(10):963–970
Oteri F, Nadalin F, Champeimont R, Carbone A (2017) BIS2Analyzer: a server for co-evolution analysis of conserved protein families. Nucleic Acids Res 45(W1):W307–W314. https://doi.org/10.1093/nar/gkx336
Park JT, Raychaudhuri D, Li H, Normark S, Mengin-Lecreulx D (1998) MppA, a periplasmic binding protein essential for import of the bacterial cell wall peptide L-alanyl-gamma-D-glutamyl-meso-diaminopimelate. J Bacteriol 180(5):1215–1223. https://doi.org/10.1128/JB.180.5.1215-1223.1998
Parra-Lopez C, Baer MT, Groisman EA (1993) Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J 12(11):4053–4062
Paterson JK, Shukla S, Black CM, Tachiwada T, Garfield S, Wincovitch S, Ernst DN, Agadir A, Li X, Ambudkar SV (2007) Human ABCB6 localizes to both the outer mitochondrial membrane and the plasma membrane. Biochemistry 46(33):9443–9452
Patzer SI, Hantke K (1998) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28(6):1199–1210. https://doi.org/10.1046/j.1365-2958.1998.00883.x
Perez C, Gerber S, Boilevin J, Bucher M, Darbre T, Aebi M, Reymond J-L, Locher KP (2015) Structure and mechanism of an active lipid-linked oligosaccharide flippase. Nature 524(7566):433–438
Phillips RB, Zimmerman A, Noakes MA, Palti Y, Morasch MR, Eiben L, Ristow SS, Thorgaard GH, Hansen JD (2003) Physical and genetic mapping of the rainbow trout major histocompatibility regions: evidence for duplication of the class I region. Immunogenetics 55(8):561–569
Qian H, Zhao X, Cao P, Lei J, Yan N, Gong X (2017) Structure of the human lipid exporter ABCA1. Cell 169(7):1228–1239 e1210. https://doi.org/10.1016/j.cell.2017.05.020
Qu L, Jiang Y, Cheng C, Wu D, Meng B, Chen Z, Zhu Y, Shaw N, Ouyang S, Liu ZJ (2018) Crystal structure of ATP-bound human ABCF1 demonstrates a unique conformation of ABC proteins. Structure 26(9):1259–1265 e1253. https://doi.org/10.1016/j.str.2018.05.019
Quazi F, Lenevich S, Molday RS (2012) ABCA4 is an N-retinylidene-phosphatidylethanolamine and phosphatidylethanolamine importer. Nat Commun 3:925. https://doi.org/10.1038/ncomms1927
Quentin Y, Fichant G, Denizot F (1999) Inventory, assembly and analysis of Bacillus subtilis ABC transport systems. J Mol Biol 287(3):467–484
Rajagopala SV, Sikorski P, Kumar A, Mosca R, Vlasblom J, Arnold R, Franca-Koh J, Pakala SB, Phanse S, Ceol A, Hauser R, Siszler G, Wuchty S, Emili A, Babu M, Aloy P, Pieper R, Uetz P (2014) The binary protein-protein interaction landscape of Escherichia coli. Nat Biotechnol 32(3):285–290. https://doi.org/10.1038/nbt.2831
Ramakrishnan V, White SW (1998) Ribosomal protein structures: insights into the architecture, machinery and evolution of the ribosome. Trends Biochem Sci 23(6):208–212. https://doi.org/10.1016/s0968-0004(98)01214-6
Rempel S, Stanek WK, Slotboom DJ (2019) ECF-type ATP-binding cassette transporters. Annu Rev Biochem 88:551–576. https://doi.org/10.1146/annurev-biochem-013118-111705
Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, Lok S, Plavsic N, Chou JL et al (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245(4922):1066–1073
Rodionov DA, Hebbeln P, Gelfand MS, Eitinger T (2006) Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J Bacteriol 188(1):317–327
Rodionov DA, Hebbeln P, Eudes A, Ter Beek J, Rodionova IA, Erkens GB, Slotboom DJ, Gelfand MS, Osterman AL, Hanson AD (2009) A novel class of modular transporters for vitamins in prokaryotes. J Bacteriol 191(1):42–51
Rodriguez GM, Smith I (2006) Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J Bacteriol 188(2):424–430
Saier MH Jr (2000) Families of transmembrane sugar transport proteins: microreview. Mol Microbiol 35(4):699–710
Saier MH Jr, Reddy VS, Tamang DG, Västermark A (2014) The transporter classification database. Nucleic Acids Res 42(Database issue):D251–D258. https://doi.org/10.1093/nar/gkt1097
Saier MH Jr, Reddy VS, Tsu BV, Ahmed MS, Li C, Moreno-Hagelsieb G (2016) The Transporter Classification Database (TCDB): recent advances. Nucleic Acids Res 44(D1):D372–D379. https://doi.org/10.1093/nar/gkv1103
Sakahira H, Nagata S (2002) Co-translational folding of caspase-activated DNase with Hsp70, Hsp40, and inhibitor of caspase-activated DNase. J Biol Chem 277(5):3364–3370. https://doi.org/10.1074/jbc.M110071200
Saurin W, Koster W, Dassa E (1994) Bacterial binding protein-dependent permeases: characterization of distinctive signatures for functionally related integral cytoplasmic membrane proteins. Mol Microbiol 12(6):993–1004
Saurin W, Hofnung M, Dassa E (1999) Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J Mol Evol 48(1):22–41
Schulz H, Fabianek RA, Pellicioli EC, Hennecke H, Thöny-Meyer L (1999) Heme transfer to the heme chaperone CcmE during cytochrome c maturation requires the CcmC protein, which may function independently of the ABC-transporter CcmAB. Proc Natl Acad Sci U S A 96(11):6462–6467. https://doi.org/10.1073/pnas.96.11.6462
Setyawati I, Stanek WK, Majsnerowska M, Swier L, Pardon E, Steyaert J, Guskov A, Slotboom DJ (2020) In vitro reconstitution of dynamically interacting integral membrane subunits of energy-coupling factor transporters. elife 9:e64389. https://doi.org/10.7554/eLife.64389
Sharma S, Davis JA, Ayvaz T, Traxler B, Davidson AL (2005) Functional reassembly of the Escherichia coli maltose transporter following purification of a MalF-MalG subassembly. J Bacteriol 187(8):2908–2911. https://doi.org/10.1128/JB.187.8.2908-2911.2005
Sharom FJ (2006) Shedding light on drug transport: structure and function of the P-glycoprotein multidrug transporter (ABCB1). Biochem Cell Biol 84(6):979–992
Shiber A, Doring K, Friedrich U, Klann K, Merker D, Zedan M, Tippmann F, Kramer G, Bukau B (2018) Cotranslational assembly of protein complexes in eukaryotes revealed by ribosome profiling. Nature 561(7722):268–272. https://doi.org/10.1038/s41586-018-0462-y
Shieh YW, Minguez P, Bork P, Auburger JJ, Guilbride DL, Kramer G, Bukau B (2015) Operon structure and cotranslational subunit association direct protein assembly in bacteria. Science 350(6261):678–680. https://doi.org/10.1126/science.aac8171
Shum M, Shintre CA, Althoff T, Gutierrez V, Segawa M, Saxberg AD, Martinez M, Adamson R, Young MR, Faust B, Gharakhanian R, Su S, Chella Krishnan K, Mahdaviani K, Veliova M, Wolf DM, Ngo J, Nocito L, Stiles L, Abramson J, Lusis AJ, Hevener AL, Zoghbi ME, Carpenter EP, Liesa M (2021) ABCB10 exports mitochondrial biliverdin, driving metabolic maladaptation in obesity. Sci Transl Med 13(594). https://doi.org/10.1126/scitranslmed.abd1869
Siche S, Neubauer O, Hebbeln P, Eitinger T (2010) A bipartite S unit of an ECF-type cobalt transporter. Res Microbiol 161(10):824–829
Simpson BW, Owens TW, Orabella MJ, Davis RM, May JM, Trauger SA, Kahne D, Ruiz N (2016) Identification of residues in the lipopolysaccharide ABC transporter that coordinate ATPase activity with extractor function. mBio 7(5):e01729-16. https://doi.org/10.1128/mBio.01729-16
Sirko A, Hryniewicz M, Hulanicka D, Böck A (1990) Sulfate and thiosulfate transport in Escherichia coli K-12: nucleotide sequence and expression of the cysTWAM gene cluster. J Bacteriol 172(6):3351–3357. https://doi.org/10.1128/jb.172.6.3351-3357.1990
Slotboom DJ (2014) Structural and mechanistic insights into prokaryotic energy-coupling factor transporters. Nat Rev Microbiol 12(2):79–87
Stamm LV, Young NR, Frye JG (1996) Sequences of the Salmonella typhimurium mglA and mglC genes. Gene 171(1):131–132. https://doi.org/10.1016/0378-1119(96)00072-8
Staudenmaier H, Van Hove B, Yaraghi Z, Braun V (1989) Nucleotide sequences of the fecBCDE genes and locations of the proteins suggest a periplasmic-binding-protein-dependent transport mechanism for iron(III) dicitrate in Escherichia coli. J Bacteriol 171(5):2626–2633. https://doi.org/10.1128/jb.171.5.2626-2633.1989
Stieger B (2009) Recent insights into the function and regulation of the bile salt export pump (ABCB11). Curr Opin Lipidol 20(3):176–181
Stoffler G, Rudloff V, Wittman HG (1968) Ribosomal proteins. 3. Preparative separation of Escherichia coli and yeast ribosomal proteins by means of gel filtration. Mol Gen Genet 101(1):70–81. https://doi.org/10.1007/BF00434813
Swier LJ, Guskov A, Slotboom DJ (2016) Structural insight in the toppling mechanism of an energy-coupling factor transporter. Nat Commun 7(1):1–11
Tan M-F, Gao T, Liu W-Q, Zhang C-Y, Yang X, Zhu J-W, Teng M-Y, Li L, Zhou R (2015) MsmK, an ATPase, contributes to utilization of multiple carbohydrates and host colonization of Streptococcus suis. PLoS One 10(7):e0130792
Tang X, Chang S, Luo Q, Zhang Z, Qiao W, Xu C, Zhang C, Niu Y, Yang W, Wang T, Zhang Z, Zhu X, Wei X, Dong C, Zhang X, Dong H (2019) Cryo-EM structures of lipopolysaccharide transporter LptB2FGC in lipopolysaccharide or AMP-PNP-bound states reveal its transport mechanism. Nat Commun 10(1):4175. https://doi.org/10.1038/s41467-019-11977-1
Tang X, Chang S, Zhang K, Luo Q, Zhang Z, Wang T, Qiao W, Wang C, Shen C, Zhang Z, Zhu X, Wei X, Dong C, Zhang X, Dong H (2021) Structural basis for bacterial lipoprotein relocation by the transporter LolCDE. Nat Struct Mol Biol 28(4):347–355. https://doi.org/10.1038/s41594-021-00573-x
Taylor NMI, Manolaridis I, Jackson SM, Kowal J, Stahlberg H, Locher KP (2017) Structure of the human multidrug transporter ABCG2. Nature 546(7659):504–509. https://doi.org/10.1038/nature22345
ter Beek J, Duurkens RH, Erkens GB, Slotboom DJ (2011) Quaternary structure and functional unit of energy coupling factor (ECF)-type transporters. J Biol Chem 286(7):5471–5475
Thélot F, Orlando BJ, Li Y, Liao M (2020) High-resolution views of lipopolysaccharide translocation driven by ABC transporters MsbA and LptB(2)FGC. Curr Opin Struct Biol 63:26–33. https://doi.org/10.1016/j.sbi.2020.03.005
Thomas GH (2010) Homes for the orphans: utilization of multiple substrate-binding proteins by ABC transporters. Mol Microbiol 75(1):6–9. https://doi.org/10.1111/j.1365-2958.2009.06961.x
Thomas C, Aller SG, Beis K, Carpenter EP, Chang G, Chen L, Dassa E, Dean M, Duong Van Hoa F, Ekiert D, Ford R, Gaudet R, Gong X, Holland IB, Huang Y, Kahne DK, Kato H, Koronakis V, Koth CM, Lee Y, Lewinson O, Lill R, Martinoia E, Murakami S, Pinkett HW, Poolman B, Rosenbaum D, Sarkadi B, Schmitt L, Schneider E, Shi Y, Shyng SL, Slotboom DJ, Tajkhorshid E, Tieleman DP, Ueda K, Varadi A, Wen PC, Yan N, Zhang P, Zheng H, Zimmer J, Tampe R (2020) Structural and functional diversity calls for a new classification of ABC transporters. FEBS Lett 594(23):3767–3775. https://doi.org/10.1002/1873-3468.13935
Thonghin N, Kargas V, Clews J, Ford RC (2018) Cryo-electron microscopy of membrane proteins. Methods 147:176–186. https://doi.org/10.1016/j.ymeth.2018.04.018
Tsou AY, Ransom SC, Gerlt JA, Buechter DD, Babbitt PC, Kenyon GL (1990) Mandelate pathway of Pseudomonas putida: sequence relationships involving mandelate racemase, (S)-mandelate dehydrogenase, and benzoylformate decarboxylase and expression of benzoylformate decarboxylase in Escherichia coli. Biochemistry 29(42):9856–9862. https://doi.org/10.1021/bi00494a015
van der Ploeg JR, Weiss MA, Saller E, Nashimoto H, Saito N, Kertesz MA, Leisinger T (1996) Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source. J Bacteriol 178(18):5438–5446. https://doi.org/10.1128/jb.178.18.5438-5446.1996
Wang T, Fu G, Pan X, Wu J, Gong X, Wang J, Shi Y (2013) Structure of a bacterial energy-coupling factor transporter. Nature 497(7448):272–276
Wang Z, Zhang M, Shi X, Xiang Q (2017) Purification and characterization of an ATPase GsiA from Salmonella enterica. Biomed Res Int 2017:3076091. https://doi.org/10.1155/2017/3076091
Ward A, Reyes CL, Yu J, Roth CB, Chang G (2007) Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc Natl Acad Sci U S A 104(48):19005–19010
Xie T, Zhang Z, Fang Q, Du B, Gong X (2021) Structural basis of substrate recognition and translocation by human ABCA4. Nat Commun 12(1):3853. https://doi.org/10.1038/s41467-021-24194-6
Xu K, Zhang M, Zhao Q, Yu F, Guo H, Wang C, He F, Ding J, Zhang P (2013) Crystal structure of a folate energy-coupling factor transporter from Lactobacillus brevis. Nature 497(7448):268–271
Yee K, Robinson C, Hurlock G, Moss RB, Wine JJ (2000) Novel cystic fibrosis mutation L1093P: Functional analysis and possible Native American origin. Hum Mutat 15(2):208–208
Yonath A, Harms J, Hansen HA, Bashan A, Schlunzen F, Levin I, Koelln I, Tocilj A, Agmon I, Peretz M, Bartels H, Bennett WS, Krumbholz S, Janell D, Weinstein S, Auerbach T, Avila H, Piolleti M, Morlang S, Franceschi F (1998) Crystallographic studies on the ribosome, a large macromolecular assembly exhibiting severe nonisomorphism, extreme beam sensitivity and no internal symmetry. Acta Crystallogr A 54(Pt 6 Pt 1):945–955. https://doi.org/10.1107/s010876739800991x
Yu Y, Zhou M, Kirsch F, Xu C, Zhang L, Wang Y, Jiang Z, Wang N, Li J, Eitinger T (2014) Planar substrate-binding site dictates the specificity of ECF-type nickel/cobalt transporters. Cell Res 24(3):267–277
Zhang P, Wang J, Shi Y (2010) Structure and mechanism of the S component of a bacterial ECF transporter. Nature 468(7324):717–720
Zhang M, Bao Z, Zhao Q, Guo H, Xu K, Wang C, Zhang P (2014) Structure of a pantothenate transporter and implications for ECF module sharing and energy coupling of group II ECF transporters. Proc Natl Acad Sci U S A 111(52):18560–18565
Zhou Z, White KA, Polissi A, Georgopoulos C, Raetz CR (1998) Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J Biol Chem 273(20):12466–12475
Zhou C, Shi H, Zhang M, Zhou L, Xiao L, Feng S, Im W, Zhou M, Zhang X, Huang Y (2021) Structural insight into phospholipid transport by the MlaFEBD complex from P. aeruginosa. J Mol Biol 433(13):166986. https://doi.org/10.1016/j.jmb.2021.166986
Zutz A, Gompf S, Schägger H, Tampé R (2009) Mitochondrial ABC proteins in health and disease. Biochim Biophys Acta Bioenerg 1787(6):681–690
Acknowledgements
We are grateful to Dr. Kostas Beis (ICSTM, UK) for helpful discussion and for kindly allowing insights into the SbmA structure ahead of publication. We would also like to thank Profs. Lutz Schmitt (Heinrich Heine University, Germany) and Ian Collinson (Bristol University, UK) for answering basic questions about ABC transporters and insertion machinery with equanimity. Lastly, we thank Dr. Steve Prince for reading this chapter prior to submission and Robin Harris for his editing of the book. Iqra Younus is a recipient of a PEEF (Punjab Educational Endowment Fund) scholarship.
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Younus, I., Kochkina, S., Choi, C.C., Sun, W., Ford, R.C. (2022). ATP-Binding Cassette Transporters: Snap-on Complexes?. In: Harris, J.R., Marles-Wright, J. (eds) Macromolecular Protein Complexes IV. Subcellular Biochemistry, vol 99. Springer, Cham. https://doi.org/10.1007/978-3-031-00793-4_2
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