1932

Abstract

Energy-coupling factor (ECF)–type ATP-binding cassette (ABC) transporters catalyze membrane transport of micronutrients in prokaryotes. Crystal structures and biochemical characterization have revealed that ECF transporters are mechanistically distinct from other ABC transport systems. Notably, ECF transporters make use of small integral membrane subunits (S-components) that are predicted to topple over in the membrane when carrying the bound substrate from the extracellular side of the bilayer to the cytosol. Here, we review the phylogenetic diversity of ECF transporters as well as recent structural and biochemical advancements that have led to the postulation of conceptually different mechanistic models. These models can be described as power stroke and thermal ratchet. Structural data indicate that the lipid composition and bilayer structure are likely to have great impact on the transport function. We argue that study of ECF transporters could lead to generic insight into membrane protein structure, dynamics, and interaction.

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2019-06-20
2024-05-29
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Literature Cited

  1. 1. 
    Henderson GB, Huennekens FM 1974. Transport of folate compounds into Lactobacillus casei. Arch. Biochem. . Biophys 164:2722–28
    [Google Scholar]
  2. 2. 
    Henderson GB, Zevely EM, Huennekens FM 1976. Folate transport in Lactobacillus casei: solubilization and general properties of the binding protein. Biochem. Biophys. Res. Commun. 68:3712–17
    [Google Scholar]
  3. 3. 
    Henderson GB, Zevely EM 1977. Purification and properties of a membrane-associated, protein from Lactobacillus casei. J. Biol. . Chem 252:3760–65
    [Google Scholar]
  4. 4. 
    Henderson GB, Zevely EM, Kadner RJ, Huennekens FM 1977. The folate and thiamine transport proteins of Lactobacillus casei. J. Supramol. . Struct 6:2239–47
    [Google Scholar]
  5. 5. 
    Henderson GB, Zevely EM 1978. Binding and transport of thiamine by Lactobacillus casei. J. . Bacteriol 133:31190–96
    [Google Scholar]
  6. 6. 
    Henderson GB, Zevely EM, Huennekens FM 1979. Coupling of energy to folate transport in Lactobacillus casei. J. . Bacteriol 139:2552–59
    [Google Scholar]
  7. 7. 
    Henderson GB, Zevely EM, Huennekens FM 1979. Mechanism of folate transport in Lactobacillus casei: evidence for a component shared with the thiamine and biotin transport systems. J. Bacteriol. 137:31308–14
    [Google Scholar]
  8. 8. 
    Henderson GB, Potuznik S 1982. Cation-dependent binding of substrate to the folate transport protein of Lactobacillus casei cation-dependent binding of substrate to the folate transport protein of Lactobacillus casei. J. . Bacteriol 150:31098–102
    [Google Scholar]
  9. 9. 
    Henderson GB, Kojima JM, Kumar HP 1985. Differential interaction of cations with the thiamine and biotin transport proteins of Lactobacillus casei. Biochim. Biophys. . Acta 813:2201–6
    [Google Scholar]
  10. 10. 
    Henderson GB, Kojima JM, Kumar HP 1985. Kinetic evidence for two interconvertible forms of the folate transport protein from Lactobacillus casei. J. . Bacteriol 163:31147–52
    [Google Scholar]
  11. 11. 
    Ames GF-L, Lever J 1970. Components of histidine transport: histidine-binding proteins and hisP protein. PNAS 66:41096–103
    [Google Scholar]
  12. 12. 
    Ferro-Luzzi Ames G, Mimura CS, Shyamala V 1990. Bacterial periplasmic permeases belong to a family of transport proteins operating from Escherichia coli to human: traffic ATPases. FEMS Microbiol. Lett. 75:4429–46
    [Google Scholar]
  13. 13. 
    Rodionov DA, Hebbeln P, Eudes A, ter Beek J, Rodionova IA et al. 2009. A novel class of modular transporters for vitamins in prokaryotes. J. Bacteriol. 91:142–51
    [Google Scholar]
  14. 14. 
    Entcheva P, Phillips DA, Streit WR 2002. Functional analysis of Sinorhizobium meliloti genes involved in biotin synthesis and transport. Appl. Environ. Microbiol. 68:62843–48
    [Google Scholar]
  15. 15. 
    Rodionov D, Hebbeln P 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. 188:1317–27
    [Google Scholar]
  16. 16. 
    Hebbeln P, Rodionov DA, Alfandega A, Eitinger T 2007. Biotin uptake in prokaryotes by solute transporters with an optional ATP-binding cassette-containing module. PNAS 104:82909–14
    [Google Scholar]
  17. 17. 
    Davidson AL, Dassa E, Orelle C, Chen J 2008. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72:2317–64
    [Google Scholar]
  18. 18. 
    Gelfand MS, Mironov AA, Jomantas J, Kozlov YI, Perumov DA 1999. A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes. Trends Genet 15:439–42
    [Google Scholar]
  19. 19. 
    Kreneva RA, Gel'fand MS, Mironov AA, Yomantas YA, Kozlov YI et al. 2000. Inactivation of the ypaA gene in Bacillus subtilis; analysis of the resulting phenotypic expression. Russ. J. Genet. 36:8972–74
    [Google Scholar]
  20. 20. 
    Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS 2002. Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms. J. Biol. Chem. 277:5048949–59
    [Google Scholar]
  21. 21. 
    Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS 2003. Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J. Biol. Chem. 278:4241148–59
    [Google Scholar]
  22. 22. 
    Burgess CM, Slotboom DJ, Eric R, Duurkens RH, Poolman B et al. 2006. The riboflavin transporter RibU in Lactococcus lactis: molecular characterization of gene expression and the transport mechanism. J. Bacteriol. 188:82752–60
    [Google Scholar]
  23. 23. 
    Duurkens RH, Tol MB, Geertsma ER, Permentier HP, Slotboom DJ 2007. Flavin binding to the high affinity riboflavin transporter RibU. J. Biol. Chem. 282:1410380–86
    [Google Scholar]
  24. 24. 
    Vogl C, Grill S, Schilling O, Stülke J, Mack M, Stolz J 2007. Characterization of riboflavin (vitamin B2) transport proteins from Bacillus subtilis and Corynebacterium glutamicum. J. . Bacteriol 189:207367–75
    [Google Scholar]
  25. 25. 
    Zhang P, Wang J, Shi Y 2010. Structure and mechanism of the S component of a bacterial ECF transporter. Nature 468:7324717–20
    [Google Scholar]
  26. 26. 
    Eudes A, Erkens GB, Slotboom DJ, Rodionov DA, Naponelli V, Hanson AD 2008. Identification of genes encoding the folate- and thiamine-binding membrane proteins in Firmicutes. J. Bacteriol. 190:227591–94
    [Google Scholar]
  27. 27. 
    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. 35:3–67
    [Google Scholar]
  28. 28. 
    Slotboom DJ. 2014. Structural and mechanistic insights into prokaryotic energy-coupling factor transporters. Nat. Rev. Microbiol. 12:279–87
    [Google Scholar]
  29. 29. 
    Finkenwirth F, Kirsch F, Eitinger T 2013. Solitary bio Y proteins mediate biotin transport into recombinant Escherichia coli. J. . Bacteriol 195:184105–11
    [Google Scholar]
  30. 30. 
    Rempel S, Colucci E, de Gier JW, Guskov A, Slotboom DJ 2018. Cysteine-mediated decyanation of vitamin B12 by the predicted membrane transporter BtuM. Nat. Commun. 9:3038
    [Google Scholar]
  31. 31. 
    Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY et al. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33:175691–702
    [Google Scholar]
  32. 32. 
    Santos JA, Rempel S, Mous STM, Pereira CT, ter Beek J et al. 2018. Functional and structural characterization of an ECF-type ABC transporter for vitamin B12. eLife 7:e35828
    [Google Scholar]
  33. 33. 
    Light SH, Su L, Rivera-Lugo R, Cornejo JA, Louie A, et al 2018. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. Nature 562:140–44
    [Google Scholar]
  34. 34. 
    Xu K, Zhang M, Zhao Q, Yu F, Guo H et al. 2013. Crystal structure of a folate energy-coupling factor transporter from Lactobacillus brevis. . Nature 497:7448268–71
    [Google Scholar]
  35. 35. 
    Wang T, Fu G, Pan X, Wu J, Gong X et al. 2013. Structure of a bacterial energy-coupling factor transporter. Nature 497:7448272–76
    [Google Scholar]
  36. 36. 
    Zhang M, Bao Z, Zhao Q, Guo H, Xu K et al. 2014. Structure of a pantothenate transporter and implications for ECF module sharing and energy coupling of group II ECF transporters. PNAS 111:5218560–65
    [Google Scholar]
  37. 37. 
    Swier LJYM, Guskov A, Slotboom DJ 2016. Structural insight in the toppling mechanism of an energy-coupling factor transporter. Nat. Commun. 7:11072
    [Google Scholar]
  38. 38. 
    Bao Z, Qi X, Hong S, Xu K, He F et al. 2017. Structure and mechanism of a group-I cobalt energy coupling factor transporter. Cell Res 27:5675–87
    [Google Scholar]
  39. 39. 
    Karpowich NK, Song JM, Cocco N, Wang DN 2015. ATP binding drives substrate capture in an ECF transporter by a release-and-catch mechanism. Nat. Struct. Mol. Biol. 22:7565–71
    [Google Scholar]
  40. 40. 
    Erkens GB, Berntsson RPA, Fulyani F, Majsnerowska M, Vujiĉić-Žagar A et al. 2011. The structural basis of modularity in ECF-type ABC transporters. Nat. Struct. Mol. Biol. 18:7755–60
    [Google Scholar]
  41. 41. 
    Berntsson RP-A, ter Beek J, Majsnerowska M, Duurkens RH, Puri P et al. 2012. Structural divergence of paralogous S components from ECF-type ABC transporters. PNAS 109:3513990–95
    [Google Scholar]
  42. 42. 
    Yu Y, Zhou M, Kirsch F, Xu C, Zhang L et al. 2014. Planar substrate-binding site dictates the specificity of ECF-type nickel/cobalt transporters. Cell Res 24:3267–77
    [Google Scholar]
  43. 43. 
    Zhao Q, Wang C, Wang C, Guo H, Bao Z et al. 2015. Structures of FolT in substrate-bound and substrate-released conformations reveal a gating mechanism for ECF transporters. Nat. Commun. 6:7661
    [Google Scholar]
  44. 44. 
    Karpowich NK, Song J, Wang DN 2016. An aromatic cap seals the substrate binding site in an ECF-type S subunit for riboflavin. J. Mol. Biol. 428:153118–30
    [Google Scholar]
  45. 45. 
    Josts I, Almeida Hernandez Y, Andreeva A, Tidow H 2016. Crystal structure of a group I energy coupling factor vitamin transporter S component in complex with its cognate substrate. Cell Chem. Biol. 23:7827–36
    [Google Scholar]
  46. 46. 
    Karpowich NK, Wang D-N 2013. Assembly and mechanism of a group II ECF transporter. PNAS 110:72534–39
    [Google Scholar]
  47. 47. 
    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. 286:75471–75
    [Google Scholar]
  48. 48. 
    Erkens GB, Slotboom DJ 2010. Biochemical characterization of ThiT from Lactococcus lactis: a thiamin transporter with picomolar substrate binding affinity. Biochemistry 49:143203–12
    [Google Scholar]
  49. 49. 
    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 6:12e29087
    [Google Scholar]
  50. 50. 
    Finkenwirth F, Neubauer O, Gunzenhäuser J, Schoknecht J, Scolari S et al. 2010. Subunit composition of an energy-coupling-factor-type biotin transporter analysed in living bacteria. Biochem. J. 431:3373–80
    [Google Scholar]
  51. 51. 
    Kirsch F, Frielingsdorf S, Pohlmann A, Eitinger T, Ziomkowska J, Herrmann A 2012. Essential amino acid residues of BioY reveal that dimers are the functional S unit of the Rhodobacter capsulatus biotin transporter. J. Bacteriol. 194:174505–12
    [Google Scholar]
  52. 52. 
    Erkens GB, Majsnerowska M, ter Beek J, Slotboom DJ 2012. Energy coupling factor-type ABC transporters for vitamin uptake in prokaryotes. Biochemistry 51:224390–96
    [Google Scholar]
  53. 53. 
    ter Beek J, Guskov A, Slotboom DJ 2014. Structural diversity of ABC transporters. J. Gen. Physiol. 143:4419–35
    [Google Scholar]
  54. 54. 
    Rees DC, Johnson E, Lewinson O 2009. ABC transporters: The power to change. Nat. Rev. Mol. Cell Biol. 10:218–27
    [Google Scholar]
  55. 55. 
    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. 19:4395–402
    [Google Scholar]
  56. 56. 
    Procko E, O'Mara ML, Bennett WFD, Tieleman DP, Gaudet R 2009. The mechanism of ABC transporters: general lessons from structural and functional studies of an antigenic peptide transporter. FASEB J 23:51287–1302
    [Google Scholar]
  57. 57. 
    Lubelski J, Van Merkerk R, Konings WN, Driessen AJM 2006. Nucleotide-binding sites of the heterodimeric LmrCD ABC-multidrug transporter of Lactococcus lactis are asymmetric. Biochemistry 45:2648–56
    [Google Scholar]
  58. 58. 
    Tsai M-F, Li M, Hwang T-C 2010. Stable ATP binding mediated by a partial NBD dimer of the CFTR chloride channel. J. Gen. Physiol 135:5399–414
    [Google Scholar]
  59. 59. 
    Csanády L. 2010. Degenerate ABC composite site is stably glued together by trapped ATP. J. Gen. Physiol. 135:5395–98
    [Google Scholar]
  60. 60. 
    Basso C, Vergani P, Nairn AC, Gadsby DC 2003. Prolonged nonhydrolytic interaction of nucleotide with CFTR's NH2-terminal nucleotide binding domain and its role in channel gating. J. Gen. Physiol. 122:3333–48
    [Google Scholar]
  61. 61. 
    Perria CL, Rajamanickam V, Lapinski PE, Raghavan M 2006. Catalytic site modifications of TAP1 and TAP2 and their functional consequences. J. Biol. Chem. 281:5239839–51
    [Google Scholar]
  62. 62. 
    Oldham ML, Chen J 2011. Snapshots of the maltose transporter during ATP hydrolysis. PNAS 108:3715152–56
    [Google Scholar]
  63. 63. 
    Finkenwirth F, Sippach M, Landmesser H, Kirsch F, Ogienko A et al. 2015. ATP-dependent conformational changes trigger substrate capture and release by an ECF-type biotin transporter. J. Biol. Chem. 290:2716929–42
    [Google Scholar]
  64. 64. 
    Finkenwirth F, Kirsch F, Eitinger T 2017. Complex stability during the transport cycle of a subclass I ECF transporter. Biochemistry 56:344578–83
    [Google Scholar]
  65. 65. 
    Oldham ML, Chen J 2011. Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science 332:60341202–5
    [Google Scholar]
  66. 66. 
    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. 191:216482–88
    [Google Scholar]
  67. 67. 
    Chen S, Oldham ML, Davidson AL, Chen J 2013. Carbon catabolite repression of the maltose transporter revealed by X-ray crystallography. Nature 499:7458364–68
    [Google Scholar]
  68. 68. 
    Böhm A, Diez J, Diederichs K, Welte W, Boos W 2002. Structural model of MalK, the ABC subunit of the maltose transporter of Escherichia coli: implications for mal gene regulation, inducer exclusion, and subunit assembly. J. Biol. Chem. 277:53708–17
    [Google Scholar]
  69. 69. 
    Yu J, Ge J, Heuveling J, Schneider E, Yang M 2015. Structural basis for substrate specificity of an amino acid ABC transporter. PNAS 112:165243–48
    [Google Scholar]
  70. 70. 
    Lewinson O, Lee AT, Locher KP, Rees DC 2010. A distinct mechanism for the ABC transporter BtuCD–BtuF revealed by the dynamics of complex formation. Nat. Struct. Mol. Biol. 17:3332–38
    [Google Scholar]
  71. 71. 
    Dawson RJP, Hollenstein K, Locher KP 2007. Uptake or extrusion: Crystal structures of full ABC transporters suggest a common mechanism. Mol. Microbiol. 65:250–57
    [Google Scholar]
  72. 72. 
    Majsnerowska M, Hänelt I, Wunnicke D, Schäfer LV, Steinhoff HJ, Slotboom DJ 2013. Substrate-induced conformational changes in the S-component ThiT from an energy coupling factor transporter. Structure 21:5861–67
    [Google Scholar]
  73. 73. 
    Swier LJYM, Monjas L, Guskov A, de Voogd AR, Erkens GB et al. 2015. Structure-based design of potent small-molecule binders to the S-component of the ECF transporter for thiamine. ChemBioChem 16:5819–26
    [Google Scholar]
  74. 74. 
    Monjas L, Swier LJYM, Setyawati I, Slotboom DJ, Hirsch AKH 2017. Dynamic combinatorial chemistry to identify binders of ThiT, an S-component of the energy-coupling factor transporter for thiamine. ChemMedChem 12:201693–96
    [Google Scholar]
  75. 75. 
    Lohse J, Swier LJYM, Oudshoorn RC, Médard G, Kuster B et al. 2017. Targeted diazotransfer reagents enable selective modification of proteins with azides. Bioconjug. Chem. 28:4913–17
    [Google Scholar]
  76. 76. 
    Zhao H, Piszczek G, Schuck P 2015. SEDPHAT—a platform for global ITC analysis and global multi-method analysis of molecular interactions. Methods 76:137–48
    [Google Scholar]
  77. 77. 
    Jardetzky O. 1966. Simple allosteric model for membrane pumps. Nature 211:969–70
    [Google Scholar]
  78. 78. 
    Drew D, Boudker O 2016. Shared molecular mechanisms of membrane transporters. Annu. Rev. Biochem. 85:543–72
    [Google Scholar]
  79. 79. 
    Reyes N, Ginter C, Boudker O 2009. Transport mechanism of a bacterial homologue of glutamate transporters. Nature 462:7275880–85
    [Google Scholar]
  80. 80. 
    Jensen S, Guskov A, Rempel S, Hänelt I, Slotboom DJ 2013. Crystal structure of a substrate-free aspartate transporter. Nat. Struct. Mol. Biol. 20:101224–27
    [Google Scholar]
  81. 81. 
    Wöhlert D, Grötzinger MJ, Kühlbrandt W, Yildiz Ö 2015. Mechanism of Na+-dependent citrate transport from the structure of an asymmetrical CitS dimer. eLife 4:e09375
    [Google Scholar]
  82. 82. 
    Lolkema JS, Slotboom DJ 2017. Structure and elevator mechanism of the Na+-citrate transporter CitS. Curr. Opin. Struct. Biol. 45:1–9
    [Google Scholar]
  83. 83. 
    Mulligan C, Fenollar-Ferrer C, Fitzgerald GA, Vergara-Jaque A, Kaufmann D et al. 2016. The bacterial dicarboxylate transporter VcINDY uses a two-domain elevator-type mechanism. Nat. Struct. Mol. Biol. 23:3256–63
    [Google Scholar]
  84. 84. 
    Garaeva AA, Oostergetel GT, Gati C, Guskov A, Paulino C, Slotboom DJ 2018. Cryo-EM structure of the human neutral amino acid transporter ASCT2. Nat. Struct. Mol. Biol. 25:515–21
    [Google Scholar]
  85. 85. 
    Lee C, Kang HJ, von Ballmoos C, Newstead S, Uzdavinys P et al. 2013. A two-domain elevator mechanism for sodium/proton antiport. Nature 501:7468573–77
    [Google Scholar]
  86. 86. 
    Kleiger G, Grothe R, Mallick P, Eisenberg D 2002. GXXXG and AXXXA: common α-helical interaction motifs in proteins, particularly in extremophiles. Biochemistry 41:195990–97
    [Google Scholar]
  87. 87. 
    Chen J. 2013. Molecular mechanism of the Escherichia coli maltose transporter. Curr. Opin. Struct. Biol. 23:4492–98
    [Google Scholar]
  88. 88. 
    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). PLOS ONE 7:9e46052
    [Google Scholar]
  89. 89. 
    Di Girolamo PM, Kadner RJ, Bradbeer C 1971. Isolation of vitamin B12 transport mutants of Escherichia coli. J. . Bacteriol 106:3751–57
    [Google Scholar]
  90. 90. 
    Choi-Rhee E, Cronan JE 2005. Biotin synthase is catalytic in vivo, but catalysis engenders destruction of the protein. Chem. Biol. 12:4461–68
    [Google Scholar]
  91. 91. 
    Kirsch F, Eitinger T 2014. Transport of nickel and cobalt ions into bacterial cells by S components of ECF transporters. BioMetals 27:4653–60
    [Google Scholar]
  92. 92. 
    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 54:314763–66
    [Google Scholar]
  93. 93. 
    Higgins CF, Ames GF 1981. Two periplasmic transport proteins which interact with a common membrane receptor show extensive homology: complete nucleotide sequences. PNAS 78:106038–42
    [Google Scholar]
  94. 94. 
    Fulyani F, Schuurman-Wolters GK, Žagar AV, Guskov A, Slotboom DJ, Poolman B 2013. Functional diversity of tandem substrate-binding domains in ABC transporters from pathogenic bacteria. Structure 21:101879–88
    [Google Scholar]
  95. 95. 
    Gouridis G, Schuurman-Wolters GK, Ploetz E, Husada F, Vietrov R et al. 2015. Conformational dynamics in substrate-binding domains influences transport in the ABC importer GlnPQ. Nat. Struct. Mol. Biol. 22:157–64
    [Google Scholar]
  96. 96. 
    Ghimire-Rijal S, Lu X, Myles DA, Cuneo MJ 2014. Duplication of genes in an ATP-binding cassette transport system increases dynamic range while maintaining ligand specificity. J. Biol. Chem. 289:4330090–100
    [Google Scholar]
  97. 97. 
    Parcej D, Tampé R 2010. ABC proteins in antigen translocation and viral inhibition. Nat. Chem. Biol. 6:572–80
    [Google Scholar]
  98. 98. 
    George AM, Jones PM 2012. Perspectives on the structure–function of ABC transporters: the switch and constant contact models. Prog. Biophys. Mol. Biol. 109:95–107
    [Google Scholar]
  99. 99. 
    Lewis VG, Ween MP, McDevitt CA 2012. The role of ATP-binding cassette transporters in bacterial pathogenicity. Protoplasma 249:919–42
    [Google Scholar]
  100. 100. 
    Chen Y, Clarke OB, Kim J, Stowe S, Kim YK et al. 2016. Structure of the STRA6 receptor for retinol uptake. Science 353:6302aad8266
    [Google Scholar]
  101. 101. 
    Allegretti M, Klusch N, Mills DJ, Vonck J, Kühlbrandt W, Davies KM 2015. Horizontal membrane-intrinsic α-helices in the stator a-subunit of an F-type ATP synthase. Nature 521:7551237–40
    [Google Scholar]
  102. 102. 
    Hahn A, Vonck J, Mills DJ, Meier T, Kuhlbrandt W 2018. Structure, mechanism, and regulation of the chloroplast ATP synthase. Science 360:6389eaat4318
    [Google Scholar]
  103. 103. 
    Bowie JU. 2013. Membrane protein twists and turns. Nature 339:398–99
    [Google Scholar]
  104. 104. 
    von Heijne G. 2006. Membrane–protein topology. Nat. Rev. Mol. Cell Biol. 7:909–18
    [Google Scholar]
  105. 105. 
    Nooren IMA, Thornton JM 2003. Diversity of protein–protein interactions. EMBO J 22:3486–92
    [Google Scholar]
  106. 106. 
    Perkins JR, Diboun I, Dessailly BH, Lees JG, Orengo C 2010. Transient protein-protein interactions: structural, functional, and network properties. Structure 18:1233–43
    [Google Scholar]
  107. 107. 
    Lemmon MA, Flanagan JM, Hunt JF, Adair BD, Bormann BJ et al. 1992. Glycophorin A dimerization is driven by specific interactions between transmembrane α-helices. J. Biol. Chem. 267:117683–89
    [Google Scholar]
  108. 108. 
    Brosig B, Langosch D 2008. The dimerization motif of the glycophorin A transmembrane segment in membranes: importance of glycine residues. Protein Sci 7:41052–56
    [Google Scholar]
  109. 109. 
    Senes A, Engel DE, Degrado WF 2004. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14:465–79
    [Google Scholar]
  110. 110. 
    Robertson JL, Kolmakova-Partensky L, Miller C 2010. Design, function and structure of a monomeric ClC transporter. Nature 468:7325844–47
    [Google Scholar]
  111. 111. 
    Last NB, Miller C 2015. Functional monomerization of a ClC-type fluoride transporter. J. Mol. Biol. 427:223607–12
    [Google Scholar]
  112. 112. 
    Kebbel F, Kurz M, Arheit M, Grütter MG, Stahlberg H 2013. Structure and substrate-induced conformational changes of the secondary citrate/sodium symporter CitS revealed by electron crystallography. Structure 21:71243–50
    [Google Scholar]
  113. 113. 
    Erkens GB, Hänelt I, Goudsmits JMH, Slotboom DJ, van Oijen AM 2013. Unsynchronised subunit motion in single trimeric sodium-coupled aspartate transporters. Nature 502:119–23
    [Google Scholar]
  114. 114. 
    Higgins CF. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67–113
    [Google Scholar]
  115. 115. 
    Wang H, Oster G 2002. Ratchets, power strokes, and molecular motors. Appl. Phys. A 75:2315–23
    [Google Scholar]
  116. 116. 
    Wagoner JA, Dill KA 2016. Molecular motors: power strokes outperform Brownian ratchets. J. Phys. Chem. B 120:266327–36
    [Google Scholar]
  117. 117. 
    Greene NP, Kaplan E, Crow A, Koronakis V 2018. Antibiotic resistance mediated by the MacB ABC transporter family: a structural and functional perspective. Front. Microbiol. 9:950
    [Google Scholar]
  118. 118. 
    Maruyama Y, Itoh T, Kaneko A, Nishitani Y, Mikami B et al. 2015. Structure of a bacterial ABC transporter involved in the import of an acidic polysaccharide alginate. Structure 23:91643–54
    [Google Scholar]
  119. 119. 
    Hvorup RN, Goetz BA, Niederer M, Hollenstein K, Perozo E, Locher KP 2007. Asymmetry in the structure of the ABC transporter-binding protein complex BtuCD-BtuF. Science 317:58431387–90
    [Google Scholar]
  120. 120. 
    Dawson RJP, Locher KP 2006. Structure of a bacterial multidrug ABC transporter. Nature 443:7108180–85
    [Google Scholar]
  121. 121. 
    Lee J-Y, Kinch LN, Borek DM, Wang J, Wang J et al. 2016. Crystal structure of the human sterol transporter ABCG5/ABCG8. Nature 533:561–64
    [Google Scholar]
  122. 122. 
    Luo Q, Yang X, Yu S, Shi H, Wang K et al. 2017. Structural basis for lipopolysaccharide extraction by ABC transporter LptB2FG. Nat. Struct. Mol. Biol. 24:5469–74
    [Google Scholar]
  123. 123. 
    Crow A, Greene NP, Kaplan E, Koronakis V 2017. Structure and mechanotransmission mechanism of the MacB ABC transporter superfamily. PNAS 114:12572–77
    [Google Scholar]
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