Skip to main content
SpringerLink
Log in

Secondary Active Transporters

  • Chapter
  • First Online:
Bacterial Cell Walls and Membranes

Part of the book series: Subcellular Biochemistry ((SCBI,volume 92))

Abstract

Transport of solutes across biological membranes is essential for cellular life. This process is mediated by membrane transport proteins which move nutrients, waste products, certain drugs and ions into and out of cells. Secondary active transporters couple the transport of substrates against their concentration gradients with the transport of other solutes down their concentration gradients. The alternating access model of membrane transporters and the coupling mechanism of secondary active transporters are introduced in this book chapter. Structural studies have identified typical protein folds for transporters that we exemplify by the major facilitator superfamily (MFS) and LeuT folds. Finally, substrate binding and substrate translocation of the transporters LacY of the MFS and AdiC of the amino acid-polyamine-organocation (APC) superfamily are described.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abramson J, Wright EM (2009) Structure and function of Na+-symporters with inverted repeats. Curr Opin Struct Biol 19:425–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610–615

    Article  CAS  PubMed  Google Scholar 

  • Andersson M, Bondar A-N, Freites JA, Tobias DJ, Kaback HR, White SH (2012) Proton-coupled dynamics in lactose permease. Structure 20:1893–1904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blattner FR (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462

    Article  CAS  PubMed  Google Scholar 

  • Boggavarapu R, Jeckelmann J-M, Harder D, Ucurum Z, Fotiadis D (2015) Role of electrostatic interactions for ligand recognition and specificity of peptide transporters. BMC Biol 13:58

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Busch W, Saier MH (2008) The transporter classification (TC) system, 2002. Crit Rev Biochem Mol Biol 37:287–337

    Article  Google Scholar 

  • Carrasco N, Antes LM, Poonian MS, Kaback HR (1986a) Lac permease of Escherichia coli: histidine-322 and glutamic acid-325 may be components of a charge-relay system. Biochemistry 25:4486–4488

    Article  CAS  PubMed  Google Scholar 

  • Carrasco N, Puttner IB, Antes LM, Lee JA, Larigan JD, Lolkema JS, Roepe PD, Kaback HR (1986b) Characterization of site-directed mutants in the lac permease of Escherichia coli. 2. Glutamate-325 replacements. Biochemistry 28:2533–2539

    Article  Google Scholar 

  • Casagrande F, Ratera M, Schenk AD, Chami M, Valencia E, Lopez JM, Torrents D, Engel A, Palacin M, Fotiadis D (2008) Projection structure of a member of the amino acid/polyamine/organocation transporter superfamily. J Biol Chem 283:33240–33248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaptal V, Kwon S, Sawaya MR, Guan L, Kaback HR, Abramson J (2011) Crystal structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition. Proc Natl Acad Sci USA 108:9361–9366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dang S, Sun L, Huang Y, Lu F, Liu Y, Gong H, Wang J, Yan N (2010) Structure of a fucose transporter in an outward-open conformation. Nature 467:734–738

    Article  CAS  PubMed  Google Scholar 

  • Doki S, Kato HE, Solcan N, Iwaki M, Koyama M, Hattori M, Iwase N, Tsukazaki T, Sugita Y, Kandori H, Newstead S, Ishitani R, Nureki O (2013) Structural basis for dynamic mechanism of proton-coupled symport by the peptide transporter POT. Proc Natl Acad Sci USA 110:11343–11348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dougherty DA (1996) Cation–π interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271:163–168

    Article  CAS  PubMed  Google Scholar 

  • Dougherty DA (2013) The Cation–π interaction. Acc Chem Res 46:885–893

    Article  CAS  PubMed  Google Scholar 

  • Drew D, Boudker O (2016) Shared molecular mechanisms of membrane transporters. Annu Rev Biochem 85:543–572

    Article  CAS  PubMed  Google Scholar 

  • Erni B (2013) The bacterial phosphoenolpyruvate: sugar phosphotransferase system (PTS): an interface between energy and signal transduction. J Iran Chem Soc 10:593–630

    Article  CAS  Google Scholar 

  • Ethayathulla AS, Yousef MS, Amin A, Leblanc G, Kaback HR, Guan L (2014) Structure-based mechanism for Na+/melibiose symport by MelB. Nat Commun 5:3009

    Article  PubMed  CAS  Google Scholar 

  • Fang Y, Jayaram H, Shane T, Kolmakova-Partensky L, Wu F, Williams C, Xiong Y, Miller C (2009) Structure of a prokaryotic virtual proton pump at 3.2 Å resolution. Nature 460:1040–1043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forrest LR, Rudnick G (2009) The rocking bundle: a mechanism for ion-coupled solute flux by symmetrical transporters. Physiology 24:377–386

    Article  CAS  PubMed  Google Scholar 

  • Forrest LR, Krämer R, Ziegler C (2011) The structural basis of secondary active transport mechanisms. Biochim Biophys Acta 1807:167–188

    Article  CAS  PubMed  Google Scholar 

  • Foster JW (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Micro 2:898–907

    Article  CAS  Google Scholar 

  • Fowler PW, Orwick-Rydmark M, Radestock S, Solcan N, Dijkman PM, Lyons JA, Kwok J, Caffrey M, Watts A, Forrest LR, Newstead S (2015) Gating topology of the proton-coupled oligopeptide symporters. Structure 23:290–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frillingos S, Sahin-Tóth M, Wu J, Kaback HR (1998) Cys-scanning mutagenesis: a novel approach to structure–function relationships in polytopic membrane proteins. FASEB J 12:1281–1299

    Article  CAS  PubMed  Google Scholar 

  • Fukuda M, Takeda H, Kato HE, Doki S, Ito K, Maturana AD, Ishitani R, Nureki O (2015) Structural basis for dynamic mechanism of nitrate/nitrite antiport by NarK. Nat Commun 6:190

    Article  CAS  Google Scholar 

  • Gallivan JP, Dougherty DA (1999) Cation–π interactions in structural biology. Proc Natl Acad Sci USA 96:9459–9464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao X, Lu F, Zhou L, Dang S, Sun L, Li X, Wang J, Shi Y (2009) Structure and mechanism of an amino acid antiporter. Science 324:1565–1568

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Zhou L, Jiao X, Lu F, Yan C, Zeng X, Wang J, Shi Y (2010) Mechanism of substrate recognition and transport by an amino acid antiporter. Nature 463:828–832

    Article  CAS  PubMed  Google Scholar 

  • Griffith JK, Baker ME, Rouch DA, Page MGP, Skurray RA, Paulsen IT, Chater KF, Baldwin SA, Henderson PJF (1992) Membrane transport proteins: implications of sequence comparisons. Curr Opin Cell Biol 4:684–695

    Article  CAS  PubMed  Google Scholar 

  • Guan L, Kaback HR (2004) Binding affinity of lactose permease is not altered by the H+ electrochemical gradient. Proc Natl Acad Sci USA 101:12148–12152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan L, Kaback HR (2006) Lessons from lactose permease. Annu Rev Biophys Biomol Struct 35:67–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan L, Hu Y, Kaback HR (2003) Aromatic stacking in the sugar binding site of the lactose permease. Biochemistry 42:1377–1382

    Article  CAS  PubMed  Google Scholar 

  • Guan L, Mirza O, Verner G, Iwata S, Kaback HR (2007) Structural determination of wild-type lactose permease. Proc Natl Acad Sci USA 104:15294–15298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guettou F, Quistgaard EM, Tresaugues L, Moberg P, Jegerschold C, Zhu L, Jong AJO, Nordlund P, Löw C (2013) Structural insights into substrate recognition in proton-dependent oligopeptide transporters. EMBO Rep 14:804–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guettou F, Quistgaard EM, Raba M, Moberg P, Löw C, Nordlund P (2014) Selectivity mechanism of a bacterial homolog of the human drug-peptide transporters PepT1 and PepT2. Nat Struct Mol Biol 21:728–731

    Article  CAS  PubMed  Google Scholar 

  • Henderson PJF (1990) Proton-linked sugar transport systems in bacteria. J Bioenerg Biomembr 22:525–569

    Article  CAS  PubMed  Google Scholar 

  • Henderson PJF, Maiden MCJ (1990) Homologous sugar transport proteins in Escherichia coli and their relatives in both prokaryotes and eukaryotes. Philos Trans R Soc Lond B Biol Sci 326:391–410

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Huang C-Y, Olieric V, Ma P, Panepucci E, Diederichs K, Wang M, Caffrey M (2015) In meso in situ serial X-ray crystallography of soluble and membrane proteins. Acta Crystallogr D Biol Crystallogr 71:1238–1256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iancu CV, Zamoon J, Woo SB, Aleshin A, Choe JY (2013) Crystal structure of a glucose/H+ symporter and its mechanism of action. Proc Natl Acad Sci USA 110:17862–17867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ilgü H, Jeckelmann J-M, Gapsys V, Ucurum Z, de Groot BL, Fotiadis D (2016) Insights into the molecular basis for substrate binding and specificity of the wild-type l-arginine/agmatine antiporter AdiC. Proc Natl Acad Sci USA 113:10358–10363

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jack DL, Paulsen IT, Saier MH (2000) The amino acid/polyamine/organocation (APC) superfamily of transporters specific for amino acids, polyamines and organocations. Microbiology 146:1797–1814

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang X, Villafuerte MKR, Andersson M, White SH, Kaback HR (2014) Galactoside-binding site in LacY. Biochemistry 53:1536–1543

    Article  CAS  PubMed  Google Scholar 

  • Jiang X, Smirnova I, Kasho V, Wu J, Hirata K, Ke M, Pardon E, Steyaert J, Yan N, Kaback HR (2016) Crystal structure of a LacY-nanobody complex in a periplasmic-open conformation. Proc Natl Acad Sci USA 113:12420–12425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaback HR, Sahin-Tóth M, Weinglass AB (2001) The kamikaze approach to membrane transport. Nat Rev Mol Cell Biol 2:610–620

    Article  CAS  PubMed  Google Scholar 

  • Karpowich NK, Wang D-N (2008) Symmetric transporters for asymmetric transport. Science 321:781–782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khafizov K, Staritzbichler R, Stamm M, Forrest LR (2010) A study of the evolution of inverted-topology repeats from LeuT-fold transporters using AlignMe. Biochemistry 49:10702–10713

    Article  CAS  PubMed  Google Scholar 

  • Kowalczyk L, Ratera M, Paladino A, Bartoccioni P, Errasti-Murugarren E, Valencia E, Portella G, Bial S, Zorzano A, Fita I, Orozco M, Carpena X, Vázquez-Ibar J, Palacín M (2011) Molecular basis of substrate-induced permeation by an amino acid antiporter. Proc Natl Acad Sci USA 108:3935–3940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar H, Kasho V, Smirnova I, Finer-Moore JS, Kaback HR, Stroud RM (2014) Structure of sugar-bound LacY. Proc Natl Acad Sci USA 111:1784–1788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar H, Finer-Moore JS, Kaback HR, Stroud RM (2015) Structure of LacY with an α-substituted galactoside: connecting the binding site to the protonation site. Proc Natl Acad Sci USA 112:9004–9009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar H, Finer-Moore JS, Jiang X, Smirnova I, Kasho V, Pardon E, Steyaert J, Kaback HR, Stroud RM (2018) Crystal Structure of a ligand-bound LacY-nanobody complex. Proc Natl Acad Sci USA 115:8769–8774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyons JA, Parker JL, Solcan N, Brinth A, Li D, Shah ST, Caffrey M, Newstead S (2014) Structural basis for polyspecificity in the POT family of proton-coupled oligopeptide transporters. EMBO Rep 15:886–893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma P, Weichert D, Aleksandrov LA, Jensen TJ, Riordan JR, Liu X, Kobilka BK, Caffrey M (2017) The cubicon method for concentrating membrane proteins in the cubic mesophase. Nat Protoc 12:1745–1762

    Article  CAS  PubMed  Google Scholar 

  • Madej MG (2014) Function, structure, and evolution of the major facilitator superfamily: the LacY manifesto. Adv Biol 2014:20

    Article  CAS  Google Scholar 

  • Madej MG, Kaback HR (2013) Evolutionary mix-and-match with MFS transporters II. Proc Natl Acad Sci USA 110:4831–4838

    Article  CAS  Google Scholar 

  • Madej MG, Soro SN, Kaback HR (2012) Apo-intermediate in the transport cycle of lactose permease (LacY). Proc Natl Acad Sci USA 109:2970–2978

    Article  Google Scholar 

  • Madej MG, Dang S, Yan N, Kaback HR (2013) Evolutionary mix-and-match with MFS transporters. Proc Nat Acad Sci USA 110:5870–5874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madej MG, Sun L, Yan N, Kaback HR (2014) Functional architecture of MFS d-glucose transporters. Proc Natl Acad Sci USA 111:719–727

    Article  CAS  Google Scholar 

  • Martinez Molledo M, Quistgaard EM, Flayhan A, Pieprzyk J, Löw C (2018) Multispecific substrate recognition in a proton-dependent oligopeptide transporter. Structure 26:467–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minhas GS, Bawdon D, Herman R, Rudden M, Stone AP, James AG, Thomas GH, Newstead S (2018) Structural basis of malodour precursor transport in the human axilla. eLife 7:e34995

    Google Scholar 

  • Mirza O, Guan L, Verner G, Iwata S, Kaback HR (2006) Structural evidence for induced fit and a mechanism for sugar/H+ symport in LacY. EMBO J 25:1177–1183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagarathinam K, Nakada-Nakura Y, Parthier C, Terada T, Juge N, Jaenecke F, Liu K, Hotta Y, Miyaji T, Omote H, Iwata S, Nomura N, Stubbs MT, Tanabe M (2018) Outward open conformation of a Major Facilitator Superfamily multidrug/H+ antiporter provides insights into switching mechanism. Nat Commun 9:4005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Newstead S, Drew D, Cameron AD, Postis VLG, Xia X, Fowler PW, Ingram JC, Carpenter EP, Sansom MSP, McPherson MJ, Baldwin SA, Iwata S (2011) Crystal structure of a prokaryotic homologue of the mammalian oligopeptide-proton symporters, PepT1 and PepT2. EMBO J 30:417–426

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nie Y, Smirnova I, Kasho V, Kaback HR (2006) Energetics of ligand-induced conformational flexibility in the lactose permease of Escherichia coli. J Biol Chem 281:35779–35784

    Article  CAS  PubMed  Google Scholar 

  • Padan E, Sarkar HK, Viitanen PV, Poonian MS, Kaback HR (1985) Site-specific mutagenesis of histidine residues in the lac permease of Escherichia coli. Proc Natl Acad Sci USA 82:6765–6768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pao SS, Paulsen IT, Saier MH (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parker JL, Li C, Brinth A, Wang Z, Vogeley L, Solcan N, Ledderboge-Vucinic G, Swanson JMJ, Caffrey M, Voth GA, Newstead S (2017) Proton movement and coupling in the POT family of peptide transporters. Proc Natl Acad Sci USA 114:13182–13187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Püttner IB, Sarkar HK, Poonian MS, Kaback HR (2002) Lac permease of Escherichia coli: histidine-205 and histidine-322 play different roles in lactose/protein symport. Biochemistry 25:4483–4485

    Article  Google Scholar 

  • Quistgaard EM, Löw C, Moberg P, Tresaugues L, Nordlund P (2013) Structural basis for substrate transport in the GLUT-homology family of monosaccharide transporters. Nat Struct Mol Biol 20:766–768

    Article  CAS  PubMed  Google Scholar 

  • Quistgaard EM, Martinez Molledo M, Löw C (2017) Structure determination of a major facilitator peptide transporter: Inward facing PepTSt from Streptococcus thermophilus crystallized in space group P3121. PLoS ONE 12:e0173126

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reddy VS, Shlykov MA, Castillo R, Sun EI, Saier MH (2012) The major facilitator superfamily (MFS) revisited. FEBS J 279:2022–2035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren Q, Paulsen IT (2007) Large-scale comparative genomic analyses of cytoplasmic membrane transport systems in prokaryotes. J Mol Microbiol Biotechnol 12:165–179

    Article  CAS  PubMed  Google Scholar 

  • Robertson DE, Kaczorowski GJ, Garcia ML, Kaback HR (1980) Active transport in membrane vesicles from Escherichia coli: the electrochemical proton gradient alters the distribution of the lac carrier between two different kinetic states. Biochemistry 19:5692–5702

    Article  CAS  PubMed  Google Scholar 

  • Sahin-Tóth M, Kaback HR (2001) Arg-302 facilitates deprotonation of Glu-325 in the transport mechanism of the lactose permease from Escherichia coli. Proc Natl Acad Sci USA 98:6068–6073

    Article  PubMed  PubMed Central  Google Scholar 

  • Sahin-Tóth M, le Coutre J, Kharabi D, le Maire G, Lee JC, Kaback HR (1999) Characterization of Glu126 and Arg144, two residues that are indispensable for substrate binding in the lactose permease of Escherichia coli. Biochemistry 38:813–819

    Article  PubMed  Google Scholar 

  • Sahin-Tóth M, Karlin A, Kaback HR (2000) Unraveling the mechanism of the lactose permease of Escherichia coli. Proc Natl Acad Sci USA 97:10729–10732

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi Y (2013) Common folds and transport mechanisms of secondary active transporters. Annu Rev Biophys 42:51–72

    Article  PubMed  CAS  Google Scholar 

  • Smirnova I, Kasho V, Kaback HR (2008) Protonation and sugar binding to LacY. Proc Natl Acad Sci USA 105:8896–8901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smirnova I, Kasho V, Sugihara J, Choe J-Y, Kaback HR (2009) Residues in the H+ translocation site define the pKa for sugar binding to LacY. Biochemistry 48:8852–8860

    Article  CAS  PubMed  Google Scholar 

  • Smirnova I, Kasho V, Sugihara J, Kaback HR (2013) Trp replacements for tightly interacting Gly–Gly pairs in LacY stabilize an outward-facing conformation. Proc Natl Acad Sci USA 110:8876–8881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solcan N, Kwok J, Fowler PW, Cameron AD, Drew D, Iwata S, Newstead S (2012) Alternating access mechanism in the POT family of oligopeptide transporters. EMBO J 31:3411–3421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun L, Zeng X, Yan C, Sun X, Gong X, Rao Y, Yan N (2012) Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature 490:361–366

    Article  CAS  PubMed  Google Scholar 

  • Taniguchi R, Kato HE, Font J, Deshpande CN, Wada M, Ito K, Ishitani R, Jormakka M, Nureki O (2015) Outward- and inward-facing structures of a putative bacterial transition-metal transporter with homology to ferroportin. Nat Commun 6:8545

    Article  CAS  PubMed  Google Scholar 

  • Vastermark A, Wollwage S, Houle ME, Rio R, Saier MH (2014) Expansion of the APC superfamily of secondary carriers. Proteins 82:2797–2811

    Article  CAS  Google Scholar 

  • Vázquez-Ibar JL, Guan L, Weinglass AB, Verner G, Gordillo R, Kaback HR (2004) Sugar recognition by the lactose permease of Escherichia coli. J Biol Chem 279:49214–49221

    Article  PubMed  CAS  Google Scholar 

  • Venkatesan P, Kaback HR (1998) The substrate-binding site in the lactose permease of Escherichia coli. Proc Natl Acad Sci USA 95:9802–9807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viitanen P, Garcia ML, Foster DL, Kaczorowski GJ, Kaback HR (1983) Mechanism of lactose translocation in proteoliposomes reconstituted with lac carrier protein purified from Escherichia coli. II. Deuterium solvent isotope effects. Biochemistry 22:2531–2536

    Article  CAS  PubMed  Google Scholar 

  • Wisedchaisri G, Park M-S, Iadanza MG, Zheng H, Gonen T (2014) Proton-coupled sugar transport in the prototypical major facilitator superfamily protein XylE. Nat Commun 5:4521

    Article  CAS  PubMed  Google Scholar 

  • Wong FH, Chen JS, Reddy V, Day JL, Shlykov MA, Wakabayashi ST, Saier MH (2012) The amino acid–polyamine–organocation superfamily. J Mol Microbiol Biotechnol 22:105–113

    Article  PubMed  CAS  Google Scholar 

  • Xie H (2008) Activity assay of membrane transport proteins. Acta Biochim Biophys Sin 40:269–277

    Article  CAS  PubMed  Google Scholar 

  • Yamashita A, Singh SK, Kawate T, Jin Y, Gouaux E (2005) Crystal structure of a bacterial homologue of Na+/Cl−-dependent neurotransmitter transporters. Nature 437:215–223

    Article  CAS  PubMed  Google Scholar 

  • Yan N (2013) Structural advances for the major facilitator superfamily (MFS) transporters. Trends Biochem Sci 38:151–159

    Article  CAS  PubMed  Google Scholar 

  • Yan H, Huang W, Yan C, Gong X, Jiang S, Zhao Y, Wang J, Shi Y (2013) Structure and mechanism of a nitrate transporter. Cell Rep 3:716–723

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, He X, Szewczyk P, Nguyen T, Chang G (2006) Structure of the multidrug transporter EmrD from Escherichia coli. Science 312:741–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zacharias N, Dougherty DA (2002) Cation–π interactions in ligand recognition and catalysis. Trends Pharmacol Sci 23:281–287

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Mao G, Liu M, Zhang L, Wang X, Zhang XC (2014) Crystal structure of the E. coli peptide transporter YbgH. Structure 22:1152–1160

    Article  CAS  PubMed  Google Scholar 

  • Zheng H, Wisedchaisri G, Gonen T (2013) Crystal structure of a nitrate/nitrite exchanger. Nature 497:647–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Swiss National Centre of Competence in Research (NCCR) TransCure, Institute of Biochemistry and Molecular Medicine, University of Bern, Bühlstrasse 28, 3012, Bern, Switzerland

    Patrick D. Bosshart & Dimitrios Fotiadis

Authors
  1. Patrick D. Bosshart
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dimitrios Fotiadis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dimitrios Fotiadis .

Editor information

Editors and Affiliations

  1. Inst. of Microbiology, University of Hohenheim, Stuttgart, Germany

    Andreas Kuhn

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bosshart, P.D., Fotiadis, D. (2019). Secondary Active Transporters. In: Kuhn, A. (eds) Bacterial Cell Walls and Membranes . Subcellular Biochemistry, vol 92. Springer, Cham. https://doi.org/10.1007/978-3-030-18768-2_9

Download citation

Publish with us

Policies and ethics

Search

Navigation