1932

Abstract

The ancient and ubiquitous major facilitator superfamily (MFS) represents the largest secondary transporter family and plays a crucial role in a multitude of physiological processes. MFS proteins transport a broad spectrum of ions and solutes across membranes via facilitated diffusion, symport, or antiport. In recent years, remarkable advances in understanding the structural biology of the MFS transporters have been made. This article reviews the history, classification, and general features of the MFS proteins; summarizes recent structural progress with a focus on the sugar porter family transporters exemplified by GLUT1; and discusses the molecular mechanisms of substrate binding, alternating access, and cotransport coupling.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-060414-033901
2015-06-22
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/biophys/44/1/annurev-biophys-060414-033901.html?itemId=/content/journals/10.1146/annurev-biophys-060414-033901&mimeType=html&fmt=ahah

Literature Cited

  1. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S. 1.  2003. Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610–15 [Google Scholar]
  2. Agre P. 2.  2004. Aquaporin water channels. Biosci. Rep. 24:127–63 [Google Scholar]
  3. Almén MS, Nordström KJ, Fredriksson R, Schiöth HB. 3.  2009. Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin. BMC Biol. 7:50 [Google Scholar]
  4. Bang O, Orskov SL. 4.  1937. Variations in the permeability of the red blood cells in man, with particular reference to the conditions obtaining in pernicious anemia. J. Clin. Investig. 16:279–88 [Google Scholar]
  5. Birnbaum MJ, Haspel HC, Rosen OM. 5.  1986. Cloning and characterization of a cDNA encoding the rat brain glucose-transporter protein. PNAS 83:5784–88 [Google Scholar]
  6. Bodoy S, Fotiadis D, Stoeger C, Kanai Y, Palacín M. 6.  2013. The small SLC43 family: facilitator system l amino acid transporters and the orphan EEG1. Mol. Asp. Med. 34:638–45 [Google Scholar]
  7. Büttner M. 7.  2007. The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Lett. 581:2318–24 [Google Scholar]
  8. Cao E, Liao M, Cheng Y, Julius D. 8.  2013. TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504:113–18 [Google Scholar]
  9. Chou JY, Jun HS, Mansfield BC. 9.  2013. The SLC37 family of phosphate-linked sugar phosphate antiporters. Mol. Asp. Med. 34:601–11 [Google Scholar]
  10. Costa C, Dias PJ, Sá-Correia I, Teixeira MC. 10.  2014. MFS multidrug transporters in pathogenic fungi: Do they have real clinical impact?. Front. Physiol. 5:197 [Google Scholar]
  11. Dang S, Sun L, Huang Y, Lu F, Liu Y. 11.  et al. 2010. Structure of a fucose transporter in an outward-open conformation. Nature 467:734–38 [Google Scholar]
  12. Daniel H, Spanier B, Kottra G, Weitz D. 12.  2006. From bacteria to man: archaic proton-dependent peptide transporters at work. Physiology 21:93–102 [Google Scholar]
  13. DeLano WL. 13.  2002. The PyMOL Molecular Graphics System. http://www.pymol.org
  14. Deng D, Xu C, Sun P, Wu J, Yan C. 14.  et al. 2014. Crystal structure of the human glucose transporter GLUT1. Nature 510:121–25 [Google Scholar]
  15. Doki S, Kato HE, Solcan N, Iwaki M, Koyama M. 15.  et al. 2013. Structural basis for dynamic mechanism of proton-coupled symport by the peptide transporter POT. PNAS 110:11343–48 [Google Scholar]
  16. Dos Santos SC, Teixeira MC, Dias PJ, Sá-Correia I. 16.  2014. MFS transporters required for multidrug/multixenobiotic (MD/MX) resistance in the model yeast: understanding their physiological function through post-genomic approaches. Front. Physiol. 5:180 [Google Scholar]
  17. Ehring R, Beyreuther K, Wright JK, Overath P. 17.  1980. In vitro and in vivo products of E. coli lactose permease gene are identical. Nature 283:537–40 [Google Scholar]
  18. El-Gebali S, Bentz S, Hediger MA, Anderle P. 18.  2013. Solute carriers (SLCs) in cancer. Mol. Asp. Med. 34:719–34 [Google Scholar]
  19. Ethayathulla AS, Yousef MS, Amin A, Leblanc G, Kaback HR, Guan L. 19.  2014. Structure-based mechanism for Na+/melibiose symport by MelB. Nat. Commun. 5:3009 [Google Scholar]
  20. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY. 20.  et al. 2014. Pfam: the protein families database. Nucleic Acids Res. 42:D222–30 [Google Scholar]
  21. Fluman N, Ryan CM, Whitelegge JP, Bibi E. 21.  2012. Dissection of mechanistic principles of a secondary multidrug efflux protein. Mol. Cell 47:777–87 [Google Scholar]
  22. Forrest LR, Krämer R, Ziegler C. 22.  2011. The structural basis of secondary active transport mechanisms. Biochim. Biophys. Acta 1807:167–88 [Google Scholar]
  23. Fox CF, Carter JR, Kennedy EP. 23.  1967. Genetic control of the membrane protein component of the lactose transport system of Escherichia coli. PNAS 57:698–705 [Google Scholar]
  24. Fox CF, Kennedy EP. 24.  1965. Specific labeling and partial purification of the M protein, a component of the β-galactoside transport system of Escherichia coli. PNAS 54:891–99 [Google Scholar]
  25. Fukumoto H, Kayano T, Buse JB, Edwards Y, Pilch PF. 25.  et al. 1989. Cloning and characterization of the major insulin-responsive glucose transporter expressed in human skeletal muscle and other insulin-responsive tissues. J. Biol. Chem. 264:7776–79 [Google Scholar]
  26. Fukumoto H, Seino S, Imura H, Seino Y, Eddy RL. 26.  et al. 1988. Sequence, tissue distribution, and chromosomal localization of mRNA encoding a human glucose transporter-like protein. PNAS 85:5434–38 [Google Scholar]
  27. Gadsby DC. 27.  2009. Ion channels versus ion pumps: the principal difference, in principle. Nat. Rev. Mol. Cell Biol. 10:344–52 [Google Scholar]
  28. Gao X, Lu F, Zhou L, Dang S, Sun L. 28.  et al. 2009. Structure and mechanism of an amino acid antiporter. Science 324:1565–68 [Google Scholar]
  29. Gao X, Zhou L, Jiao X, Lu F, Yan C. 29.  et al. 2010. Mechanism of substrate recognition and transport by an amino acid antiporter. Nature 463:828–32 [Google Scholar]
  30. Guan L, Kaback HR. 30.  2006. Lessons from lactose permease. Annu. Rev. Biophys. Biomol. Struct. 35:67–91 [Google Scholar]
  31. Guettou F, Quistgaard EM, Raba M, Moberg P, Low C, Nordlund P. 31.  2014. Selectivity mechanism of a bacterial homolog of the human drug-peptide transporters PepT1 and PepT2. Nat. Struct. Mol. Biol. 21:728–31 [Google Scholar]
  32. Guettou F, Quistgaard EM, Tresaugues L, Moberg P, Jegerschold C. 32.  et al. 2013. Structural insights into substrate recognition in proton-dependent oligopeptide transporters. EMBO Rep. 14:804–10 [Google Scholar]
  33. Hagenbuch B, Stieger B. 33.  2013. The SLCO (former SLC21) superfamily of transporters. Mol. Asp. Med. 34:396–412 [Google Scholar]
  34. Halestrap AP. 34.  2013. The SLC16 gene family—structure, role and regulation in health and disease. Mol. Asp. Med. 34:337–49 [Google Scholar]
  35. He Y, Wang K, Yan N. 35.  2014. The recombinant expression systems for structure determination of eukaryotic membrane proteins. Protein Cell 5:658–72 [Google Scholar]
  36. Hediger MA. 36.  1994. Structure, function and evolution of solute transporters in prokaryotes and eukaryotes. J. Exp. Biol. 196:15–49 [Google Scholar]
  37. Hediger MA, Clémençon B, Burrier RE, Bruford EA. 37.  2013. The ABCs of membrane transporters in health and disease (SLC series): introduction. Mol. Asp. Med. 34:95–107 [Google Scholar]
  38. Henderson PJ, Maiden MC. 38.  1990. Homologous sugar transport proteins in Escherichia coli and their relatives in both prokaryotes and eukaryotes. Philos. Trans. R. Soc. Lond. B 326:391–410 [Google Scholar]
  39. Henderson PJF, Baldwin SA. 39.  2012. Structural biology: bundles of insights into sugar transporters. Nature 490:348–50 [Google Scholar]
  40. Heymann JAW, Sarker R, Hirai T, Shi D, Milne JLS. 40.  et al. 2001. Projection structure and molecular architecture of OxlT, a bacterial membrane transporter. EMBO J. 20:4408–13 [Google Scholar]
  41. Hirabayashi Y, Nomura KH, Nomura K. 41.  2013. The acetyl-CoA transporter family SLC33. Mol. Asp. Med. 34:586–89 [Google Scholar]
  42. Hirai T, Heymann JAW, Shi D, Sarker R, Maloney PC, Subramaniam S. 42.  2002. Three-dimensional structure of a bacterial oxalate transporter. Nat. Struct. Biol. 9:597–600 [Google Scholar]
  43. Hodgkin AL, Huxley AF. 43.  1945. Resting and action potentials in single nerve fibres. J. Physiol. 104:176–95 [Google Scholar]
  44. Höglund PJ, Nordström KJV, Schiöth HB, Fredriksson R. 44.  2011. The solute carrier families have a remarkably long evolutionary history with the majority of the human families present before divergence of Bilaterian species. Mol. Biol. Evol. 28:1531–41 [Google Scholar]
  45. Hruz PW, Mueckler MM. 45.  2001. Structural analysis of the GLUT1 facilitative glucose transporter. Mol. Membr. Biol. 18:183–93 [Google Scholar]
  46. Huang Y, Lemieux MJ, Song J, Auer M, Wang DN. 46.  2003. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301:616–20 [Google Scholar]
  47. Iancu CV, Zamoon J, Woo SB, Aleshin A, Choe JY. 47.  2013. Crystal structure of a glucose/H+ symporter and its mechanism of action. PNAS 110:17862–67 [Google Scholar]
  48. Jacob F, Monod J. 48.  1961. Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3:318–56 [Google Scholar]
  49. Jacob F, Perrin D, Sanchez C, Monod J. 49.  1960. Operon: a group of genes with the expression coordinated by an operator. C. R. Hebd. Seances Acad. Sci. 250:1727–29 [Google Scholar]
  50. James DE, Brown R, Navarro J, Pilch PF. 50.  1988. Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein. Nature 333:183–85 [Google Scholar]
  51. Jardetzky O. 51.  1966. Simple allosteric model for membrane pumps. Nature 211:969–70 [Google Scholar]
  52. Jiang D, Zhao Y, Wang X, Fan J, Heng J. 52.  et al. 2013. Structure of the YajR transporter suggests a transport mechanism based on the conserved motif A. PNAS 110:14664–69 [Google Scholar]
  53. Kaback HR, Sahin-Tóth M, Weinglass AB. 53.  2001. The kamikaze approach to membrane transport. Nat. Rev. Mol. Cell Biol. 2:610–20 [Google Scholar]
  54. Kaback HR, Smirnova I, Kasho V, Nie Y, Zhou Y. 54.  2011. The alternating access transport mechanism in LacY. J. Membr. Biol. 239:85–93 [Google Scholar]
  55. Kaback HR, Stadtman ER. 55.  1966. Proline uptake by an isolated cytoplasmic membrane preparation of Escherichia coli. PNAS 55:920–27 [Google Scholar]
  56. Kasahara M, Hinkle PC. 56.  1976. Reconstitution of D-glucose transport catalyzed by a protein fraction from human erythrocytes in sonicated liposomes. PNAS 73:396–400 [Google Scholar]
  57. Kasahara M, Hinkle PC. 57.  1977. Reconstitution and purification of the D-glucose transporter from human erythrocytes. J. Biol. Chem. 252:7384–90 [Google Scholar]
  58. Koepsell H. 58.  2013. The SLC22 family with transporters of organic cations, anions and zwitterions. Mol. Asp. Med. 34:413–35 [Google Scholar]
  59. Kühlbrandt W. 59.  2014. Microscopy: Cryo-EM enters a new era. eLIFE 3:e03678 [Google Scholar]
  60. Kumar H, Kasho V, Smirnova I, Finer-Moore JS, Kaback HR, Stroud RM. 60.  2014. Structure of sugar-bound LacY. PNAS 111:1784–88 [Google Scholar]
  61. Laganowsky A, Reading E, Allison TM, Ulmschneider MB, Degiacomi MT. 61.  et al. 2014. Membrane proteins bind lipids selectively to modulate their structure and function. Nature 510:172–75 [Google Scholar]
  62. Lawal HO, Krantz DE. 62.  2013. SLC18: vesicular neurotransmitter transporters for monoamines and acetylcholine. Mol. Asp. Med. 34:360–72 [Google Scholar]
  63. Lee C, Kang HJ, von Ballmoos C, Newstead S, Uzdavinys P. 63.  et al. 2013. A two-domain elevator mechanism for sodium/proton antiport. Nature 501:573–77 [Google Scholar]
  64. LeFevre PG. 64.  1948. Evidence of active transfer of certain non-electrolytes across the human red cell membrane. J. Gen. Physiol. 31:505–27 [Google Scholar]
  65. Léran S, Varala K, Boyer J-C, Chiurazzi M, Crawford N. 65.  et al. 2014. A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci. 19:5–9 [Google Scholar]
  66. Li F, Ma C, Wang X, Gao C, Zhang J. 66.  et al. 2011. Characterization of Sucrose transporter alleles and their association with seed yield-related traits in Brassica napus L. BMC Plant Biol. 11:168 [Google Scholar]
  67. Liao M, Cao E, Julius D, Cheng Y. 67.  2013. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504:107–12 [Google Scholar]
  68. Lu P, Bai XC, Ma D, Xie T, Yan C. 68.  et al. 2014. Three-dimensional structure of human γ-secretase. Nature 512:166–70 [Google Scholar]
  69. Madej MG, Sun L, Yan N, Kaback HR. 69.  2014. Functional architecture of MFS D-glucose transporters. PNAS 111:E719–27 [Google Scholar]
  70. Maiden MC, Davis EO, Baldwin SA, Moore DC, Henderson PJ. 70.  1987. Mammalian and bacterial sugar transport proteins are homologous. Nature 325:641–43 [Google Scholar]
  71. Marger MD, Saier MH Jr. 71.  1993. A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem. Sci. 18:13–20 [Google Scholar]
  72. Meyerson JR, Kumar J, Chittori S, Rao P, Pierson J. 72.  et al. 2014. Structural mechanism of glutamate receptor activation and desensitization. Nature 514:328–34 [Google Scholar]
  73. Mueckler M, Caruso C, Baldwin SA, Panico M, Blench I. 73.  et al. 1985. Sequence and structure of a human glucose transporter. Science 229:941–45 [Google Scholar]
  74. Mueckler M, Thorens B. 74.  2013. The SLC2 (GLUT) family of membrane transporters. Mol. Asp. Med. 34:121–38 [Google Scholar]
  75. Murata K, Mitsuoka K, Hirai T, Walz T, Agre P. 75.  et al. 2000. Structural determinants of water permeation through aquaporin-1. Nature 407:599–605 [Google Scholar]
  76. Newstead S. 76.  2014. Molecular insights into proton coupled peptide transport in the PTR family of oligopeptide transporters. Biochim. Biophys. Acta 1850:488–99 [Google Scholar]
  77. Newstead S, Drew D, Cameron AD, Postis VL, Xia X. 77.  et al. 2011. Crystal structure of a prokaryotic homologue of the mammalian oligopeptide–proton symporters, PepT1 and PepT2. EMBO J. 30:417–26 [Google Scholar]
  78. Nguyen LN, Ma D, Shui G, Wong P, Cazenave-Gassiot A. 78.  et al. 2014. Mfsd2a is a transporter for the essential omega-3 fatty acid docosahexaenoic acid. Nature 509:503–6 [Google Scholar]
  79. Oka Y, Asano T, Shibasaki Y, Lin J-L, Tsukuda K. 79.  et al. 1990. C-terminal truncated glucose transporter is locked into an inward-facing form without transport activity. Nature 345:550–53 [Google Scholar]
  80. Oldham ML, Chen J. 80.  2011. Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science 332:1202–5 [Google Scholar]
  81. Özcan S, Johnston M. 81.  1999. Function and regulation of yeast hexose transporters. Microbiol. Mol. Biol. Rev. 63:554–69 [Google Scholar]
  82. Parker JL, Newstead S. 82.  2014. Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507:68–72 [Google Scholar]
  83. Pedersen BP, Kumar H, Waight AB, Risenmay AJ, Roe-Zurz Z. 83.  et al. 2013. Crystal structure of a eukaryotic phosphate transporter. Nature 496:533–36 [Google Scholar]
  84. Quistgaard EM, Löw C, Moberg P, Trésaugues L, Nordlund P. 84.  2013. Structural basis for substrate transport in the GLUT-homology family of monosaccharide transporters. Nat. Struct. Mol. Biol. 20:766–68 [Google Scholar]
  85. Rask-Andersen M, Masuram S, Fredriksson R, Schiöth HB. 85.  2013. Solute carriers as drug targets: current use, clinical trials and prospective. Mol. Asp. Med. 34:702–10 [Google Scholar]
  86. Rasmussen SGF, Choi H-J, Fung JJ, Pardon E, Casarosa P. 86.  et al. 2011. Structure of a nanobody-stabilized active state of the β2 adrenoceptor. Nature 469:175–80 [Google Scholar]
  87. Reimer RJ. 87.  2013. SLC17: a functionally diverse family of organic anion transporters. Mol. Asp. Med. 34:350–59 [Google Scholar]
  88. Reyes N, Ginter C, Boudker O. 88.  2009. Transport mechanism of a bacterial homologue of glutamate transporters. Nature 462:880–85 [Google Scholar]
  89. Robertson DE, Kaczorowski GJ, Garcia ML, Kaback HR. 89.  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 19:5692–702 [Google Scholar]
  90. Saier MH Jr, Reddy VS, Tamang DG, Västermark Å. 90.  2014. The transporter classification database. Nucleic Acids Res. 42:D251–58 [Google Scholar]
  91. Sanderson NM, Qi D, Steel A, Henderson PJF. 91.  1998. Effect of the D32N and N300F mutations on the activity of the bacterial sugar transport protein, GalP. Biochem. Soc. Trans. 26:S306 [Google Scholar]
  92. Schürmann A, Doege H, Ohnimus H, Monser V, Buchs A, Joost H-G. 92.  1997. Role of conserved arginine and glutamate residues on the cytosolic surface of glucose transporters for transporter function. Biochemistry 36:12897–902 [Google Scholar]
  93. Shi Y. 93.  2013. Common folds and transport mechanisms of secondary active transporters. Annu. Rev. Biophys. 42:51–72 [Google Scholar]
  94. Shuman HA. 94.  1981. The use of gene fusions of study bacterial transport proteins. J. Membr. Biol. 61:1–11 [Google Scholar]
  95. Skou JC. 95.  1957. The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochim. Biophys. Acta 23:394–401 [Google Scholar]
  96. Smith DE, Clémençon B, Hediger MA. 96.  2013. Proton-coupled oligopeptide transporter family SLC15: physiological, pharmacological and pathological implications. Mol. Asp. Med. 34:323–36 [Google Scholar]
  97. Solcan N, Kwok J, Fowler PW, Cameron AD, Drew D. 97.  et al. 2012. Alternating access mechanism in the POT family of oligopeptide transporters. EMBO J. 31:3411–21 [Google Scholar]
  98. Steyaert J, Kobilka BK. 98.  2011. Nanobody stabilization of G protein-coupled receptor conformational states. Curr. Opin. Struct. Biol. 21:567–72 [Google Scholar]
  99. Sun J, Bankston JR, Payandeh J, Hinds TR, Zagotta WN, Zheng N. 99.  2014. Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature 507:73–77 [Google Scholar]
  100. Sun L, Zeng X, Yan C, Sun X, Gong X. 100.  et al. 2012. Crystal structure of a bacterial homologue of glucose transporters GLUT1–4. Nature 490:361–66 [Google Scholar]
  101. Thorens B, Mueckler M. 101.  2010. Glucose transporters in the 21st century. Am. J. Physiol. Endocrinol. Metab. 298:E141–45 [Google Scholar]
  102. Thorens B, Sarkar HK, Kaback HR, Lodish HF. 102.  1988. Cloning and functional expression in bacteria of a novel glucose transporter present in liver, intestine, kidney, and β-pancreatic islet cells. Cell 55:281–90 [Google Scholar]
  103. Vitavska O, Wieczorek H. 103.  2013. The SLC45 gene family of putative sugar transporters. Mol. Asp. Med. 34:655–60 [Google Scholar]
  104. Wang T, Fu G, Pan X, Wu J, Gong X. 104.  et al. 2013. Structure of a bacterial energy-coupling factor transporter. Nature 497:272–76 [Google Scholar]
  105. Wang Y, Huang Y, Wang J, Cheng C, Huang W. 105.  et al. 2009. Structure of the formate transporter FocA reveals a pentameric aquaporin-like channel. Nature 462:467–72 [Google Scholar]
  106. Widdas WF. 106.  1951. Inability of diffusion to account for placental glucose transfer in the sheep. J. Physiol. 115:36–37 [Google Scholar]
  107. Widdas WF. 107.  1952. Inability of diffusion to account for placental glucose transfer in the sheep and consideration of the kinetics of a possible carrier transfer. J. Physiol. 118:23–39 [Google Scholar]
  108. Wilbrandt W, Guensberg E, Lauener H. 108.  1947. Admission of glucose by erythrocyte membrane. Helv. Physiol. Pharmacol. Acta 5:C20–22 [Google Scholar]
  109. Wilson-O'Brien AL, Patron N, Rogers S. 109.  2010. Evolutionary ancestry and novel functions of the mammalian glucose transporter (GLUT) family. BMC Evol. Biol. 10:152 [Google Scholar]
  110. Wisedchaisri G, Park M-S, Iadanza MG, Zheng H, Gonen T. 110.  2014. Proton-coupled sugar transport in the prototypical major facilitator superfamily protein XylE. Nat. Commun. 5:4521 [Google Scholar]
  111. Wong FH, Chen JS, Reddy V, Day JL, Shlykov MA. 111.  et al. 2012. The amino acid-polyamine-organocation superfamily. J. Mol. Microbiol. Biotechnol. 22:105–13 [Google Scholar]
  112. Xu K, Zhang M, Zhao Q, Yu F, Guo H. 112.  et al. 2013. Crystal structure of a folate energy-coupling factor transporter from Lactobacillus brevis. Nature 497:268–71 [Google Scholar]
  113. Yamashita A, Singh SK, Kawate T, Jin Y, Gouaux E. 113.  2005. Crystal structure of a bacterial homologue of Na+/Cl-dependent neurotransmitter transporters. Nature 437:215–23 [Google Scholar]
  114. Yan H, Huang W, Yan C, Gong X, Jiang S. 114.  et al. 2013. Structure and mechanism of a nitrate transporter. Cell Rep. 3:716–23 [Google Scholar]
  115. Yan N. 115.  2013. Structural advances for the major facilitator superfamily (MFS) transporters. Trends Biochem. Sci. 38:151–59 [Google Scholar]
  116. Yan N. 116.  2013. Structural investigation of the proton-coupled secondary transporters. Curr. Opin. Struct. Biol. 23:483–91 [Google Scholar]
  117. Yin Y, He X, Szewczyk P, Nguyen T, Chang G. 117.  2006. Structure of the multidrug transporter EmrD from Escherichia coli. Science 312:741–44 [Google Scholar]
  118. Young JD, Yao SYM, Baldwin JM, Cass CE, Baldwin SA. 118.  2013. The human concentrative and equilibrative nucleoside transporter families, SLC28 and SLC29. Mol. Asp. Med. 34:529–47 [Google Scholar]
  119. Zhang P, Wang J, Shi Y. 119.  2010. Structure and mechanism of the S component of a bacterial ECF transporter. Nature 468:717–20 [Google Scholar]
  120. Zhao R, Goldman ID. 120.  2013. Folate and thiamine transporters mediated by facilitative carriers (SLC19A1-3 and SLC46A1) and folate receptors. Mol. Asp. Med. 34:373–85 [Google Scholar]
  121. Zhao Y, Mao G, Liu M, Zhang L, Wang X, Zhang XC. 121.  2014. Crystal structure of the E. coli peptide transporter YbgH. Structure 22:1152–60 [Google Scholar]
  122. Zheng H, Wisedchaisri G, Gonen T. 122.  2013. Crystal structure of a nitrate/nitrite exchanger. Nature 497:647–51 [Google Scholar]
  123. Zhou X, Levin EJ, Pan Y, McCoy JG, Sharma R. 123.  et al. 2014. Structural basis of the alternating-access mechanism in a bile acid transporter. Nature 505:569–73 [Google Scholar]
  124. Zhou Y, Jiang X, Kaback HR. 124.  2012. . Role of the irreplaceable residues in the LacY alternating access mechanism. PNAS 109:12438–42 [Google Scholar]
/content/journals/10.1146/annurev-biophys-060414-033901
Loading
/content/journals/10.1146/annurev-biophys-060414-033901
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error