Thermodynamics of ABC transporters

Abstract

ABC transporters form the largest of all transporter families, and their structural study has made tremendous progress over recent years. However, despite such advances, the precise mechanisms that determine the energy-coupling between ATP hydrolysis and the conformational changes following substrate binding remain to be elucidated. Here, we present our thermodynamic analysis for both ABC importers and exporters, and introduce the two new concepts of differential-binding energy and elastic conformational energy into the discussion.We hope that the structural analysis of ABC transporters will henceforth take thermodynamic aspects of transport mechanisms into account as well.

Key words： ABC transporters; differential-binding energy; energy-coupling; elastic conformational energy

References

1 Austermuhle MI, Hall JA, Klug CS, Davidson AL (2004) Maltosebinding protein is open in the catalytic transition state for ATP hydrolysis during maltose transport. J Biol Chem 279:28243–28250

2 Berntsson RP, Smits SH, Schmitt L, Slotboom DJ, Poolman B (2010)A structural classification of substrate-binding proteins. FEBS Lett 584:2606–2617

3 Bouige P, Laurent D, Piloyan L, Dassa E (2002) Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr Protein Pept Sci 3:541–559

4 Bublitz M, Morth JP, Nissen P (2011) P-type ATPases at a glance.J Cell Sci 124:2515–2519

5 Chen J (2013) Molecular mechanism of the Escherichia coli maltose transporter. Curr Opin Struct Biol 23:492–498

6 Covitz KM, Panagiotidis CH, Hor LI, Reyes M, Treptow NA, Shuman HA (1994) Mutations that alter the transmembrane signalling pathway in an ATP binding cassette (ABC) transporter. EMBO J13:1752–1759

7 Davidson AL, Shuman HA, Nikaido H (1992) Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins. Proc Natl Acad Sci USA 89:2360–2364

8 Davidson AL, Laghaeian SS, Mannering DE (1996) The maltose transport system of Escherichia coli displays positive cooperativity in ATP hydrolysis. J Biol Chem 271:4858–4863

9 Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function,and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317–364 (table of contents)

10 Deeley RG, Westlake C, Cole SP (2006) Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 86:849–899

11 Gadsby DC, Vergani P, Csanady L (2006) The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440:477–483

12 Grossmann N, Vakkasoglu AS, Hulpke S, Abele R, Gaudet R, Tampe R (2014) Mechanistic determinants of the directionality and energetics of active export by a heterodimeric ABC transporter. Nat Commun 5:5419

13 Heng J, Zhao Y, Liu M, Liu Y, Fan J, Wang X, Zhang XC (2015)Substrate-bound structure of the E. coli multidrug resistance transporter MdfA. Cell research 25:1060–1073

14 Higgins CF, Linton KJ (2004) The ATP switch model for ABC transporters. Nat Struct Mol Biol 11:918–926

15 Hollenstein K, Frei DC, Locher KP (2007) Structure of an ABC transporter in complex with its binding protein. Nature 446:213–216

16 Huang Y, Lemieux MJ, Song J, Auer M, Wang DN (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301:616–620

17 Jardetzky O (1966) Simple allosteric model for membrane pumps. Nature 211:969–970

18 Jiang D, Zhao Y, Wang X, Fan J, Heng J, Liu X, Feng W, Kang X,Huang B, Liu Jet al (2013) Structure of the YajR transporter suggests a transport mechanism based on the conserved motif A. Proc Natl Acad Sci USA 110:14664–14669

19 Jones PM, O’Mara ML, George AM (2009) ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem Sci 34:520–531

20 Kadaba NS, Kaiser JT, Johnson E, Lee A, Rees DC (2008) The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 321:250–253

21 Khare D, Oldham ML, Orelle C, Davidson AL, Chen J (2009)Alternating access in maltose transporter mediated by rigid-body rotations. Mol Cell 33:528–536

22 Kim SH, Chang AB, Saier MH Jr (2004) Sequence similarity between multidrug resistance efflux pumps of the ABC and RND superfamilies. Microbiology 150:2493–2495

23 Kim J, Wu S, Tomasiak TM, Mergel C, Winter MB, Stiller SB, Robles-Colmanares Y, Stroud RM, Tampe R, Craik CS, et al. (2014)Subnanometre-resolution electron cryomicroscopy structure of a heterodimeric ABC exporter. Nature 517:396–400

24 Korkhov VM, Mireku SA, Locher KP (2012) Structure of AMP-PNPbound vitamin B12 transporter BtuCD-F. Nature 490:367–372

25 Korkhov VM, Mireku SA, Veprintsev DB, Locher KP (2014) Structure of AMP-PNP-bound BtuCD and mechanism of ATP-powered vitamin B12 transport by BtuCD-F. Nat Struct Mol Biol 21:1097–1099

26 Li L, Sham YY, Bikadi Z, Elmquist WF (2011) pH-Dependent transport of pemetrexed by breast cancer resistance protein. Drug Metab Dispos 39:1478–1485

27 Linton KJ, Higgins CF (1998) The Escherichia coli ATP-binding cassette (ABC) proteins. Mol Microbiol 28:5–13

28 Locher KP, Lee AT, Rees DC (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296:1091–1098

29 Oldham ML, Chen J (2011) Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science 332:1202–1205

30 Oldham ML, Chen S, Chen J (2013) Structural basis for substrate specificity in the Escherichia coli maltose transport system. Proc Natl Acad Sci USA 110:18132–18137

31 Orelle C, Ayvaz T, Everly RM, Klug CS, Davidson AL (2008) Both maltose-binding protein and ATP are required for nucleotidebinding domain closure in the intact maltose ABC transporter. Proc Natl Acad Sci USA 105:12837–12842

32 Perez C, Gerber S, Boilevin J, Bucher M, Darbre T, Aebi M,Reymond JL, Locher KP (2015) Structure and mechanism of an active lipid-linked oligosaccharide flippase. Nature 524:433–438

33 Phillips R, Ursell T, Wiggins P, Sens P (2009) Emerging roles for lipids in shaping membrane-protein function. Nature 459:379–385

34 Pinkett HW, Lee AT, Lum P, Locher KP, Rees DC (2007) An inwardfacing conformation of a putative metal-chelate-type ABC transporter. Science 315:373–377

35 Poolman B, Konings WN (1993) Secondary solute transport in bacteria. Biochim Biophys Acta 1183:5–39

36 Qiao S, Luo Q, Zhao Y, Zhang XC, Huang Y (2014) Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature 511:108–111

37 Reyes CL, Chang G (2005) Structure of the ABC transporter MsbA in complex with ADP·vanadate and lipopolysaccharide. Science 308:1028–1031

38 Rice AJ, Park A, Pinkett HW (2014) Diversity in ABC transporters:type I, II and III importers. Crit Rev Biochem Mol Biol 49:426–437

39 Sauna ZE, Ambudkar SV (2000) Evidence for a requirement for ATP hydrolysis at two distinct steps during a single turnover of the catalytic cycle of human P-glycoprotein. Proc Natl Acad Sci USA 97:2515–2520

40 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 48:22–41

41 Seelig A, Blatter XL, Wohnsland F (2000) Substrate recognition by P-glycoprotein and the multidrug resistance-associated protein MRP1: a comparison. Int J Clin Pharmacol Ther 38:111–121

42 Senior AE, Al-Shawi MK, Urbatsch IL (1995) The catalytic cycle of P-glycoprotein. FEBS Lett 377:285–289

43 Sherman DJ, Lazarus MB, Murphy L, Liu C, Walker S, Ruiz N, Kahne D (2014) Decoupling catalytic activity from biological function of the ATPase that powers lipopolysaccharide transport. Proc Natl Acad Sci USA 111:4982–4987

44 Shilling R, Federici L, Walas F, Venter H, Velamakanni S, Woebking B, Balakrishnan L, Luisi B, van Veen HW (2005) A critical role of a carboxylate in proton conduction by the ATP-binding cassette multidrug transporter LmrA. FASEB J 19:1698–1700

45 Srinivasan V, Pierik AJ, Lill R (2014) Crystal structures of nucleotidefree and glutathione-bound mitochondrial ABC transporter Atm1. Science 343:1137–1140

46 Varma MV, Sarkar M, Kapoor N, Panchagnula R (2005) pHdependent functional activity of P-glycoprotein in limiting intestinal absorption of protic drugs 1. Simultaneous determination of quinidine and permeability markers in rat in situ perfusion samples. J Chromatog B Analyt Technol Biomed Life Sci 816:243–249

47 Venter H, Shilling RA, Velamakanni S, Balakrishnan L, Van Veen HW (2003) An ABC transporter with a secondary-active multidrug translocator domain. Nature 426:866–870

48 Wesolowska O (2011) Interaction of phenothiazines, stilbenes and flavonoids with multidrug resistance-associated transporters,P-glycoprotein and MRP1. Acta Biochim Pol 58:433–448

49 Woo JS, Zeltina A, Goetz BA, Locher KP (2012) X-ray structure of the Yersinia pestis heme transporter HmuUV. Nat Struct Mol Biol 19:1310–1315

50 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 497:268–271

51 Zhang DW, Gu HM, Situ D, Haimeur A, Cole SP, Deeley RG (2003)Functional importance of polar and charged amino acid residues in transmembrane helix 14 of multidrug resistance protein 1(MRP1/ABCC1): identification of an aspartate residue critical for conversion from a high to low affinity substrate binding state. J Biol Chem 278:46052–46063

52 Zhang XC, Cao C, Zhou Y, Zhao Y (2014) Proton transfer-mediated GPCR activation. Protein Cell 6:12–17

53 Zhang XC, Zhao Y, Heng J, Jiang D (2015) Energy coupling mechanisms of MFS transporters. Protein Sci.