1932

Abstract

Soluble sugars serve five main purposes in multicellular organisms: as sources of carbon skeletons, osmolytes, signals, and transient energy storage and as transport molecules. Most sugars are derived from photosynthetic organisms, particularly plants. In multicellular organisms, some cells specialize in providing sugars to other cells (e.g., intestinal and liver cells in animals, photosynthetic cells in plants), whereas others depend completely on an external supply (e.g., brain cells, roots and seeds). This cellular exchange of sugars requires transport proteins to mediate uptake or release from cells or subcellular compartments. Thus, not surprisingly, sugar transport is critical for plants, animals, and humans. At present, three classes of eukaryotic sugar transporters have been characterized, namely the glucose transporters (GLUTs), sodium-glucose symporters (SGLTs), and SWEETs. This review presents the history and state of the art of sugar transporter research, covering genetics, biochemistry, and physiology—from their identification and characterization to their structure, function, and physiology. In humans, understanding sugar transport has therapeutic importance (e.g., addressing diabetes or limiting access of cancer cells to sugars), and in plants, these transporters are critical for crop yield and pathogen susceptibility.

Keyword(s): carrierglucoseGLUTSGLTsucroseSWEET
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-060614-033904
2015-06-02
2024-04-22
Loading full text...

Full text loading...

/deliver/fulltext/biochem/84/1/annurev-biochem-060614-033904.html?itemId=/content/journals/10.1146/annurev-biochem-060614-033904&mimeType=html&fmt=ahah

Literature Cited

  1. Cori CF. 1.  1925. The fate of sugar in the animal body. I. The rate of absorption of hexoses and pentoses from the intestinal tract. J. Biol. Chem. 66:691–715 [Google Scholar]
  2. Cori CF. 2.  1926. The rate of absorption of a mixture of glucose and galactose. Proc. Soc. Exp. Biol. Med. 23:290–91 [Google Scholar]
  3. Crane RK. 3.  1965. Na+-dependent transport in the intestine and other animal tissues. Fed. Proc. 24:1000–6 [Google Scholar]
  4. Crane RK, Miller D, Bihler I. 4.  1961. The restrictions on possible mechanisms of intestinal transport of sugars. Membrane Transport and Metabolism: Proceedings of a Symposium held in Prague, August 22–27, 1960 A Kleinzeller, A Kotyk 439–49 Prague: Czech Acad. Sci. [Google Scholar]
  5. Rickenberg HV, Cohen GN, Buttin G, Monod J. 5.  1956. La galactoside—permease d'Escherichia coli. Ann. Inst. Pasteur 91:829–57 [Google Scholar]
  6. Deutscher J, Aké FMD, Derkaoui M, Zébré AC, Cao TN. 6.  et al. 2014. The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein–protein interactions. Microbiol. Mol. Biol. Rev. 78:231–56 [Google Scholar]
  7. Kaback HR, Smirnova I, Kasho V, Nie Y, Zhou Y. 7.  2011. The alternating access transport mechanism in LacY. J. Membr. Biol. 239:85–93 [Google Scholar]
  8. Wright EM, Loo DDF, Hirayama BA. 8.  2011. Biology of human sodium glucose transporters. Physiol. Rev. 91:733–94 [Google Scholar]
  9. Thorens B, Mueckler M. 9.  2010. Glucose transporters in the 21st century. Am. J. Physiol. Endocrinol. Metab. 298:E141–45 [Google Scholar]
  10. Guan L, Kaback HR. 10.  2006. Lessons from lactose permease. Annu. Rev. Biophys. Biomol. Struct. 35:67–91 [Google Scholar]
  11. Raja M, Puntheeranurak T, Hinterdorfer P, Kinne R. 11.  2012. SLC5 and SLC2 transporters in epithelia—cellular role and molecular mechanisms. Curr. Top. Membr. 70:29–76 [Google Scholar]
  12. Kundig W, Ghosch S, Roseman S. 12.  1964. Phosphate bound to histidine in a protein as an intermediate in a novel phosphotransferase system. PNAS 52:1067–74 [Google Scholar]
  13. Clore GM, Venditti V. 13.  2013. Structure, dynamics and biophysics of the cytoplasmic protein–protein complexes of the bacterial phosphoenolpyruvate:sugar phosphotransferase system. Trends Biochem. Sci. 38:515–30 [Google Scholar]
  14. Saier MH, Hvorup RN, Barabote RD. 14.  2005. Evolution of the bacterial phosphotransferase system: from carriers and enzymes to group translocators. Biochem. Soc. Trans. 33:220–24 [Google Scholar]
  15. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML. 15.  et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–32 [Google Scholar]
  16. Dutrochet BJH. 16.  1824. Recherches anatomiques et physiologiques sur la structure intime des animaux et des végétaux Paris: Bailliere
  17. Nägeli C, Cramer C. 17.  1855. Pflanzenphysiologische Untersuchungen, Heft 1 Zürich: Schultess [Google Scholar]
  18. Robertson D. 18.  1957. New observations on the ultrastructure of the membranes of frog peripheral nerve fibers. J. Biophys. Biochem. Cytol. 3:1043–48 [Google Scholar]
  19. Smith HW. 19.  1962. The plasma membrane, with notes on the history of botany. Circulation 26:987–1012 [Google Scholar]
  20. Malinsky J, Opekarová M, Grossmann G, Tanner W. 20.  2013. Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu. Rev. Plant. Biol. 64:501–29 [Google Scholar]
  21. Kleinzeller A. 21.  1997. Ernest Overton's contribution to the cell membrane concept: a centennial appreciation. News Physiol. Sci. 12:49–53 [Google Scholar]
  22. Overton E. 22.  1895. Über die osmotischen Eigenschaften der lebenden Pflanzen- und Tierzelle. Vierteljahr. Naturforsch. Ges. Zürich 40:159–201 [Google Scholar]
  23. Collander R. 23.  1937. The permeability of plant protoplasts to non-electrolytes. Trans. Faraday Soc. 33:985–90 [Google Scholar]
  24. Höber R, Höber J. 24.  1937. Experiments on the absorption of organic solutes in the small intestine of rats. J. Cell Comp. Physiol. 10:401–22 [Google Scholar]
  25. Jacobs MH, Stewart DR. 25.  1946. Observations on an oligodynamic action of copper on human erythrocytes. Am. J. Med. Sci. 211:246 [Google Scholar]
  26. LeFevre PG. 26.  1948. Evidence of active transfer of certain non-electrolytes across the human red cell membrane. J. Gen. Physiol. 31:505–27 [Google Scholar]
  27. Macey RI, Farmer RE. 27.  1970. Inhibition of water and solute permeability in human red cells. Biochim. Biophys. Acta 211:104–6 [Google Scholar]
  28. Fu D, Libson A, Miercke LJ, Weitzman C, Nollert P. 28.  et al. 2000. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290:481–86 [Google Scholar]
  29. Fox CF, Kennedy EP. 29.  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]
  30. Sistrom WR. 30.  1958. On the physical state of the intracellularly accumulated substrates of β-galactoside-permease in Escherichia coli. Biochim. Biophys. Acta 29:579–87 [Google Scholar]
  31. Wilson TH, Crane RK. 31.  1958. The specificity of sugar transport by hamster intestine. Biochim. Biophys. Acta 29:30–32 [Google Scholar]
  32. Komor E, Tanner W. 32.  1971. Characterization of the active hexose transport system of Chlorella vulgaris. Biochim. Biophys. Acta 241:170–79 [Google Scholar]
  33. Mitchell P. 33.  1963. Molecule group and electron translocation through natural membranes. Biochem. Soc. Symp. 22:142–68 [Google Scholar]
  34. Bihler I, Crane RK. 34.  1962. Studies on the mechanism of intestinal absorption of sugars. V. The influence of several cations and anions on the active transport of sugars, in vitro, by various preparations of hamster small intestine. Biochim. Biophys. Acta 59:78–93 [Google Scholar]
  35. West IC. 35.  1970. Lactose transport coupled to proton movements in Escherichia coli. Biochem. Biophys. Res. Commun. 41:655–61 [Google Scholar]
  36. Komor E. 36.  1973. Proton-coupled hexose transport in Chlorella vulgaris. FEBS Lett. 38:16–18 [Google Scholar]
  37. Komor E, Tanner W. 37.  1974. The hexose–proton symport system of Chlorella vulgaris. Specificity, stoichiometry and energetics of sugar-induced proton uptake. Eur. J. Biochem. 44:219–23 [Google Scholar]
  38. Konings WN, Hellingwerf KJ, Elferink MGL. 38.  1984. The interaction between electron transfer, proton motive force and solute transport in bacteria. Antonie van Leeuwenhoek 50:545–55 [Google Scholar]
  39. Eddy AA, Seaston A, Gardner D, Hacking C. 39.  1980. Thermodynamic efficiency of cotransport mechanisms with special reference to proton and anion transport in yeast. Ann. N.Y. Acad. Sci. 341:494–509 [Google Scholar]
  40. Reinhold L, Kaplan A. 40.  1984. Membrane transport of sugars and amino acids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 35:45–83 [Google Scholar]
  41. Schultz SG, Curran PF. 41.  1970. Coupled transport of sodium and organic solutes. Physiol. Rev. 50:637–718 [Google Scholar]
  42. Ullrich KJ. 42.  1979. Sugar, amino acid, and Na+ cotransport in the proximal tubule. Annu. Rev. Physiol. 41:181–95 [Google Scholar]
  43. Winkler HH, Wilson TH. 43.  1966. The role of energy coupling in the transport of β-galactosides by Escherichia coli. J. Biol. Chem. 241:2200–11 [Google Scholar]
  44. Büchel DE, Gronenborn B, Müller-Hill B. 44.  1980. Sequence of the lactose permease gene. Nature 283:541–45 [Google Scholar]
  45. Lewis DA, Bisson LF. 45.  1991. The HXT1 gene product of Saccharomyces cerevisiae is a new member of the family of hexose transporters. Mol. Cell Biol. 11:3804–13 [Google Scholar]
  46. Mueckler M, Caruso C, Baldwin SA, Panico M, Blench I. 46.  et al. 1985. Sequence and structure of a human glucose transporter. Science 229:941–45 [Google Scholar]
  47. Hediger MA, Coady MJ, Ikeda TS, Wright EM. 47.  1987. Expression cloning and cDNA sequencing of the Na+/glucose co-transporter. Nature 330:379–81 [Google Scholar]
  48. Celenza JL, Marshall-Carlson L, Carlson M. 48.  1988. The yeast snf3 gene encodes a glucose transporter homologous to the mammalian protein. PNAS 85:2130–34 [Google Scholar]
  49. Sauer N, Tanner W. 49.  1989. The hexose carrier from Chlorella. cDNA cloning of a eucaryotic H+ cotransporter. FEBS Lett. 259:43–46 [Google Scholar]
  50. Riesmeier JW, Willmitzer L, Frommer WB. 50.  1992. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 11:4705–13 [Google Scholar]
  51. Newman MJ, Foster DL, Wilson TH, Kaback HR. 51.  1981. Purification and reconstitution of functional lactose carrier from Escherichia coli. J. Biol. Chem. 256:11804–8 [Google Scholar]
  52. Kim EJ, Kwak JM, Uozumi N, Schroeder JI. 52.  1998. AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell 10:51–62 [Google Scholar]
  53. Xu Y, Tao Y, Cheung L, Fan C, Chen L-Q. 53.  et al. 2014. Structures of bacterial homologues of SWEET transporters in two distinct conformations. Nature 515:448–52 [Google Scholar]
  54. Wang J, Yan C, Li Y, Hirata K, Yamamoto M. 54.  et al. 2014. Crystal structure of a bacterial homologue of SWEET transporters. Cell Res. 24:1486–89 [Google Scholar]
  55. Sun L, Zeng X, Yan C, Sun X, Gong X. 55.  et al. 2012. Crystal structure of a bacterial homologue of glucose transporters GLUT1–4. Nature 490:361–66 [Google Scholar]
  56. Loo DDF, Hirayama BA, Karakossian MH, Meinild A-K, Wright EM. 56.  2006. Conformational dynamics of hSGLT1 during Na+/glucose cotransport. J. Gen. Physiol. 128:701–20 [Google Scholar]
  57. Nour-Eldin HH, Andersen TG, Burow M, Madsen SR, Jørgensen ME. 57.  et al. 2012. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488:531–34 [Google Scholar]
  58. Dulla C, Tani H, Okumoto S, Frommer WB, Reimer RJ, Huguenard JR. 58.  2008. Imaging of glutamate in brain slices using FRET sensors. J. Neurosci. Methods 168:306–19 [Google Scholar]
  59. Chaudhuri B, Hörmann F, Lalonde S, Brady SM, Orlando DA. 59.  et al. 2008. Protonophore- and pH-insensitive glucose and sucrose accumulation detected by FRET nanosensors in Arabidopsis root tips. Plant J. 56:948–62 [Google Scholar]
  60. Chaudhuri B, Hörmann F, Frommer WB. 60.  2011. Dynamic imaging of glucose flux impedance using FRET sensors in wild-type Arabidopsis plants. J. Exp. Bot. 62:2411–17 [Google Scholar]
  61. Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S. 61.  et al. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–11 [Google Scholar]
  62. De Michele R, Ast C, Loque D, Ho CH, Andrade SL. 62.  et al. 2013. Fluorescent sensors reporting the activity of ammonium transceptors in live cells. eLife 2:e00800 [Google Scholar]
  63. Ho CH, Frommer WB. 63.  2014. Fluorescent sensors for activity and regulation of the nitrate transceptor CHL1/NRT1.1 and oligopeptide transporters. eLife 3:e01917 [Google Scholar]
  64. Sauer N, Friedländer K, Gräml-Wicke U. 64.  1990. Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana. EMBO J. 9:3045–50 [Google Scholar]
  65. Riesmeier JW, Hirner B, Frommer WB. 65.  1993. Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell 5:1591–98 [Google Scholar]
  66. Kasahara M, Hinkle PC. 66.  1976. Reconstitution of d-glucose transport catalyzed by a protein fraction from human erythrocytes in sonicated liposomes. PNAS 73:396–400 [Google Scholar]
  67. Horiba N, Masuda S, Ohnishi C, Takeuchi D, Okuda M, Inui K. 67.  2003. Na+-dependent fructose transport via rNaGLT1 in rat kidney. FEBS Lett. 546:276–80 [Google Scholar]
  68. Horiba N, Masuda S, Takeuchi A, Takeuchi D, Okuda M, Inui K. 68.  2003. Cloning and characterization of a novel Na+-dependent glucose transporter (NaGLT1) in rat kidney. J. Biol. Chem. 278:14669–76 [Google Scholar]
  69. Sosso D, Chen LQ, Frommer WB. 69.  2013. The SWEET glucoside transporter family. Encyclopedia of Biophysics G Roberts 52556–58 Berlin: Springer [Google Scholar]
  70. Mueckler M, Thorens B. 70.  2013. The SLC2 (GLUT) family of membrane transporters. Mol. Aspects Med. 34:121–38 [Google Scholar]
  71. Chardon F, Bedu M, Calenge F, Klemens PA, Spinner L. 71.  et al. 2013. Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr. Biol. 23:697–702 [Google Scholar]
  72. Guo WJ, Nagy R, Chen HY, Pfrunder S, Yu YC. 72.  et al. 2013. SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol. 164:777–89 [Google Scholar]
  73. Klemens PA, Patzke K, Deitmer JW, Spinner L, Le Hir R. 73.  et al. 2013. Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth and stress tolerance in Arabidopsis thaliana. Plant Physiol. 163:1338–52 [Google Scholar]
  74. Aluri S, Buttner M. 74.  2007. Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. PNAS 104:2537–42 [Google Scholar]
  75. Yamada K, Osakabe Y, Mizoi J, Nakashima K, Fujita Y. 75.  et al. 2010. Functional analysis of an Arabidopsis thaliana abiotic stress–inducible facilitated diffusion transporter for monosaccharides. J. Biol. Chem. 285:1138–46 [Google Scholar]
  76. Schulz A, Beyhl D, Marten I, Wormit A, Neuhaus E. 76.  et al. 2011. Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2. Plant J. 68:129–36 [Google Scholar]
  77. Bryant NJ, Govers R, James DE. 77.  2002. Regulated transport of the glucose transporter GLUT4. Nat. Rev. Mol. Cell Biol. 3:267–77 [Google Scholar]
  78. Klip A, Sun Y, Chiu TT, Foley KP. 78.  2014. Signal transduction meets vesicle traffic: the software and hardware of GLUT4 translocation. Am. J. Physiol. Cell Physiol. 306:C879–86 [Google Scholar]
  79. Holman GD, Kozka IJ, Clark AE, Flower CJ, Saltis J. 79.  et al. 1990. Cell surface labeling of glucose transporter isoform GLUT4 by bis-mannose photolabel. Correlation with stimulation of glucose transport in rat adipose cells by insulin and phorbol ester. J. Biol. Chem 265:18172–79 [Google Scholar]
  80. Maier A, Völker B, Boles E, Fuhrmann GF. 80.  2002. Characterisation of glucose transport in Saccharomyces cerevisiae with plasma membrane vesicles (countertransport) and intact cells (initial uptake) with single Hxt1, Hxt2, Hxt3, Hxt4, Hxt6, Hxt7 or Gal2 transporters. FEMS Yeast Res. 2:539–50 [Google Scholar]
  81. Reifenberger E, Boles E, Ciriacy M. 81.  1997. Kinetic characterization of individual hexose transporters of Saccharomyces cerevisiae and their relation to the triggering mechanisms of glucose repression. Eur. J. Biochem. 245:324–33 [Google Scholar]
  82. Boorer KJ, Loo DDF, Frommer WB, Wright EM. 82.  1996. Transport mechanism of the cloned potato H+/sucrose cotransporter StSUT1. J. Biol. Chem. 271:25139–44 [Google Scholar]
  83. Boorer KJ, Loo DDF, Wright EM. 83.  1994. Steady-state and presteady-state kinetics of the H+/hexose cotransporter (STP1) from Arabidopsis thaliana expressed in Xenopus oocytes. J. Biol. Chem. 269:20417–24 [Google Scholar]
  84. Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J, Hedrich R. 84.  2005. Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force. J. Biol. Chem. 280:21437–43 [Google Scholar]
  85. Carruthers A, DeZutter J, Ganguly A, Devaskar SU. 85.  2009. Will the original glucose transporter isoform please stand up!. Am. J. Physiol. Endocrinol. Metab. 297:E836–48 [Google Scholar]
  86. Neundlinger I, Puntheeranurak T, Wildling L, Rankl C, Wang L-X. 86.  et al. 2014. Forces and dynamics of glucose and inhibitor binding to sodium glucose co-transporter SGLT1 studied by single molecule force spectroscopy. J. Biol. Chem. 289:21673–83 [Google Scholar]
  87. Li JL, Tajkhorshid E. 87.  2012. A gate-free pathway for substrate release from the inward-facing state of the Na+-galactose transporter. Biochim. Biophys. Acta 1818:263–71 [Google Scholar]
  88. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S. 88.  2003. Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610–15 [Google Scholar]
  89. Frillingos S, Sahin-Toth M, Wu J, Kaback HR. 89.  1998. Cys-scanning mutagenesis: a novel approach to structure function relationships in polytopic membrane proteins. FASEB J. 12:1281–99 [Google Scholar]
  90. Mueckler M, Weng W, Kruse M. 90.  1994. Glutamine 161 of GLUT1 glucose transporter is critical for transport activity and exofacial ligand binding. J. Biol. Chem. 269:20533–38 [Google Scholar]
  91. Will A, Caspari T, Tanner W. 91.  1994. Km mutants of the Chlorella monosaccharide/H+ cotransporter randomly generated by PCR. PNAS 91:10163–67 [Google Scholar]
  92. Kumar H, Kasho V, Smirnova I, Finer-Moore JS, Kaback HR, Stroud RM. 92.  2014. Structure of sugar-bound LacY. PNAS 111:1784–88 [Google Scholar]
  93. Madej MG, Sun L, Yan N, Kaback HR. 93.  2014. Functional architecture of MFS d-glucose transporters. PNAS 111:e719–27 [Google Scholar]
  94. Deng D, Xu C, Sun P, Wu J, Yan C. 94.  et al. 2014. Crystal structure of the human glucose transporter GLUT1. Nature 510:121–25 [Google Scholar]
  95. Madej MG, Dang S, Yan N, Kaback HR. 95.  2013. Evolutionary mix-and-match with MFS transporters. PNAS 110:5870–74 [Google Scholar]
  96. Quistgaard EM, Löw C, Moberg P, Trésaugues L, Nordlund P. 96.  2013. Structural basis for substrate transport in the GLUT-homology family of monosaccharide transporters. Nat. Struct. Mol. Biol. 20:766–68 [Google Scholar]
  97. Iancu CV, Zamoon J, Woo SB, Aleshin A, Choe JY. 97.  2013. Crystal structure of a glucose/H+ symporter and its mechanism of action. PNAS 110:17862–67 [Google Scholar]
  98. Faham S, Watanabe A, Besserer GM, Cascio D, Specht A. 98.  et al. 2008. The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na+/sugar symport. Science 321:810–14 [Google Scholar]
  99. Bianchi L, Díez-Sampedro A. 99.  2010. A single amino acid change converts the sugar sensor SGLT3 into a sugar transporter. PLOS ONE 5:e10241 [Google Scholar]
  100. Watanabe A, Choe S, Chaptal V, Rosenberg JM, Wright EM. 100.  et al. 2010. The mechanism of sodium and substrate release from the binding pocket of vSGLT. Nature 468:988–91 [Google Scholar]
  101. Höglund PJ, Nordström KJ, Schiöth HB, Fredriksson R. 101.  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]
  102. Xuan YH, Hu YB, Chen LQ, Sosso D, Ducat DC. 102.  et al. 2013. Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. PNAS 110:e3685–94 [Google Scholar]
  103. Niittylä T, Fuglsang AT, Palmgren MG, Frommer WB, Schulze WX. 103.  2007. Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Mol. Cell Proteomics 6:1711–26 [Google Scholar]
  104. De Zutter JK, Levine KB, Deng D, Carruthers A. 104.  2013. Sequence determinants of GLUT1 oligomerization—analysis by homology-scanning mutagenesis. J. Biol. Chem. 288:20734–44 [Google Scholar]
  105. Lin IW, Sosso D, Chen LQ, Gase K, Kim SG. 105.  et al. 2014. Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature 508:546–49 [Google Scholar]
  106. Moitra K, Dean M. 106.  2011. Evolution of ABC transporters by gene duplication and their role in human disease. Biol. Chem. 392:29–37 [Google Scholar]
  107. Oldham ML, Chen J. 107.  2011. Snapshots of the maltose transporter during ATP hydrolysis. PNAS 108:15152–56 [Google Scholar]
  108. Khare D, Oldham ML, Orelle C, Davidson AL, Chen J. 108.  2009. Alternating access in maltose transporter mediated by rigid-body rotations. Mol. Cell 33:528–36 [Google Scholar]
  109. Oldham ML, Chen J. 109.  2011. Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science 332:1202–5 [Google Scholar]
  110. Oldham ML, Khare D, Quiocho FA, Davidson AL, Chen J. 110.  2007. Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450:515–21 [Google Scholar]
  111. Barabote RD, Saier MH Jr. 111.  2005. Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol. Mol. Biol. Rev. 69:608–34 [Google Scholar]
  112. McCoy JG, Levin EJ, Zhou M. 112.  2015. Structural insight into the PTS sugar transporter EIIC. Biochim. Biophys. Acta 1850577–85
  113. Kojima I, Nakagawa Y, Ohtsu Y, Medina A, Nagasawa M. 113.  2014. Sweet taste–sensing receptors expressed in pancreatic β-cells: SWEET molecules act as biased agonists. Endocrinol. Metab. 29:12–19 [Google Scholar]
  114. Ozcan S, Dover J, Rosenwald AG, Wölfl S, Johnston M. 114.  1996. Two glucose transporters in Saccharomyces cerevisiae are glucose sensors that generate a signal for induction of gene expression. PNAS 93:12428–32 [Google Scholar]
  115. Thevelein JM, Voordeckers K. 115.  2009. Functioning and evolutionary significance of nutrient transceptors. Mol. Biol. Evol. 26:2407–14 [Google Scholar]
  116. Barker L, Kühn C, Weise A, Schulz A, Gebhardt C. 116.  et al. 2000. SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12:1153–64 [Google Scholar]
  117. Bermejo C, Haerizadeh F, Sadoine MS, Chermak D, Frommer WB. 117.  2013. Differential regulation of glucose transport activity in yeast by specific cAMP signatures. Biochem. J. 452:489–97 [Google Scholar]
  118. Lang F, Stournaras C, Alesutan I. 118.  2014. Regulation of transport across cell membranes by the serum- and glucocorticoid-inducible kinase SGK1. Mol. Membr. Biol. 31:29–36 [Google Scholar]
  119. Devraj K, Klinger ME, Myers RL, Mokashi A, Hawkins RA, Simpson IA. 119.  2011. GLUT-1 glucose transporters in the blood–brain barrier: differential phosphorylation. J. Neurosci. Res. 89:1913–25 [Google Scholar]
  120. Ghezzi C, Wright EM. 120.  2012. Regulation of the human Na+-dependent glucose cotransporter hSGLT2. Am. J. Physiol. Cell Physiol. 303:C348–54 [Google Scholar]
  121. Takanaga H, Chaudhuri B, Frommer WB. 121.  2008. GLUT1 and GLUT9 as major contributors to glucose influx in HepG2 cells identified by a high sensitivity intramolecular FRET glucose sensor. Biochim. Biophys. Acta 1778:1091–99 [Google Scholar]
  122. Augustin R. 122.  2010. The protein family of glucose transport facilitators: It's not only about glucose after all. IUBMB Life 62:315–33 [Google Scholar]
  123. Harada N, Inagaki N. 123.  2012. Role of sodium-glucose transporters in glucose uptake of the intestine and kidney. J. Diabetes Investig. 3:352–53 [Google Scholar]
  124. Chen LQ, Lin IW, Qu XQ, Sosso D, Mcfarlane HE et al.124.  2015. Embryo nutrition by a cascade of sequentially expressed sucrose transporters in the seed coat. Plant Cell. In press
  125. Sun MX, Huang XY, Yang J, Guan YF, Yang ZN. 125.  2013. Arabidopsis RPG1 is important for primexine deposition and functions redundantly with RPG2 for plant fertility at the late reproductive stage. Plant Reprod. 26:83–91 [Google Scholar]
  126. Yang B, Sugio A, White FF. 126.  2006. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. PNAS 103:10503–8 [Google Scholar]
  127. Cohn M, Bart R, Shybut M, Dahlbeck D, Gomez M. 127.  et al. 2014. Xanthomonas axonopodis virulence is promoted by a transcription activator–like (TAL) effector–mediated induction of a SWEET sugar transporter in cassava. Mol. Plant-Microbe Interact. 27:1186–98 [Google Scholar]
  128. Tagoh H, Kishi H, Muraguchi A. 128.  1996. Molecular cloning and characterization of a novel stromal cell–derived cDNA encoding a protein that facilitates gene activation of recombination activating gene (RAG)-1 in human lymphoid progenitors. Biochem. Biophys. Res. Commun. 221:744–49 [Google Scholar]
  129. Um J-H, Brown AL, Singh SK, Chen Y, Gucek M. 129.  et al. 2013. Metabolic sensor AMPK directly phosphorylates RAG1 protein and regulates V(D)J recombination. PNAS 110:9873–78 [Google Scholar]
  130. Barnhill JC, Stokes AJ, Koblan-Huberson M, Shimoda LMN, Muraguchi A. 130.  et al. 2004. RGA protein associates with a TRPV ion channel during biosynthesis and trafficking. J. Cell Biochem. 91:808–20 [Google Scholar]
  131. Stokes AJ, Wakano C, Del Carmen KA, Koblan-Huberson M, Turner H. 131.  2005. Formation of a physiological complex between TRPV2 and RGA protein promotes cell surface expression of TRPV2. J. Cell Biochem. 94:669–83 [Google Scholar]
  132. Hisanaga E, Nagasawa M, Ueki K, Kulkarni RN, Mori M, Kojima I. 132.  2009. Regulation of calcium-permeable TRPV2 channel by insulin in pancreatic β-cells. Diabetes 58:174–84 [Google Scholar]
  133. Lalonde S, Wipf D, Frommer WB. 133.  2004. Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu. Rev. Plant Biol. 55:341–72 [Google Scholar]
  134. De Michele R, Ast C, Loque D, Ho CH, Andrade SL. 134.  et al. 2013. Fluorescent sensors reporting the activity of ammonium transceptors in live cells. eLife 2:e00800 [Google Scholar]
  135. Okumoto S, Jones A, Frommer WB. 135.  2012. Quantitative imaging with fluorescent biosensors. Annu. Rev. Plant Biol. 63:663–706 [Google Scholar]
  136. Fehr M, Lalonde S, Lager I, Wolff MW, Frommer WB. 136.  2003. In vivo imaging of the dynamics of glucose uptake in the cytosol of COS-7 cells by fluorescent nanosensors. J. Biol. Chem. 278:19127–33 [Google Scholar]
  137. Hou BH, Takanaga H, Grossmann G, Chen LQ, Qu XQ. 137.  et al. 2011. Optical sensors for monitoring dynamic changes of intracellular metabolite levels in mammalian cells. Nat. Protoc. 6:1818–33 [Google Scholar]
  138. Takanaga H, Frommer WB. 138.  2010. Facilitative plasma membrane transporters function during ER transit. FASEB J. 24:2849–58 [Google Scholar]
  139. Zambon A, Zoso A, Luni C, Frommer WB, Elvassore N. 139.  2014. Determination of glucose flux in live myoblasts by microfluidic nanosensing and mathematical modeling. Integr. Biol. Quant. Biosci. Nano Macro 6:277–88 [Google Scholar]
  140. Chen CC, Wilson TH. 140.  1984. The phospholipid requirement for activity of the lactose carrier of Escherichia coli. J. Biol. Chem. 259:10150–58 [Google Scholar]
  141. Wang X, Bogdanov M, Dowhan W. 141.  2002. Topology of polytopic membrane protein subdomains is dictated by membrane phospholipid composition. EMBO J. 21:5673–81 [Google Scholar]
  142. Chaptal V, Kwon S, Sawaya MR, Guan L, Kaback HR, Abramson J. 142.  2011. Crystal structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition. PNAS 108:9361–66 [Google Scholar]
  143. Mirza O, Guan L, Verner G, Iwata S, Kaback HR. 143.  2006. Structural evidence for induced fit and a mechanism for sugar/H+ symport in LacY. EMBO J. 25:1177–83 [Google Scholar]
  144. Guan L, Mirza O, Verner G, Iwata S, Kaback HR. 144.  2007. Structural determination of wild-type lactose permease. PNAS 104:15294–98 [Google Scholar]
  145. Chaptal V, Kwon S, Sawaya MR, Guan L, Kaback HR, Abramson J. 145.  2011. Crystal structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition. PNAS 108:9361–66 [Google Scholar]
  146. Dang S, Sun L, Huang Y, Lu F, Liu Y. 146.  et al. 2010. Structure of a fucose transporter in an outward-open conformation. Nature 467:734–38 [Google Scholar]
  147. Cao Y, Jin X, Levin EJ, Huang H, Zong Y. 147.  et al. 2011. Crystal structure of a phosphorylation-coupled saccharide transporter. Nature 473:50–54 [Google Scholar]
  148. Fanconi G, Bickel H. 148.  1949. Die chronische Aminoacidurie (Aminosäurediabetes oder nephrotisch-glukosurischer Zwergwuchs) bei der Glykogenose und der Cystinkrankheit. Helv. Paediatr. Acta 4:359–96 [Google Scholar]
  149. De Vos A, Heimberg H, Quartier E, Huypens P, Bouwens L. 149.  et al. 1995. Human and rat β cells differ in glucose transporter but not in glucokinase gene expression. J. Clin. Investig. 96:2489–95 [Google Scholar]
  150. Lisinski I, Schürmann A, Joost HG, Cushman SW, Al-Hasani H. 150.  2001. Targeting of GLUT6 (formerly GLUT9) and GLUT8 in rat adipose cells. Biochem. J. 358:517–22 [Google Scholar]
  151. Porpaczy E, Bilban M, Heinze G, Gruber M, Vanura K. 151.  et al. 2009. Gene expression signature of chronic lymphocytic leukaemia with trisomy 12. Eur. J. Clin. Investig. 39:568–75 [Google Scholar]
  152. Lin WH, Chuang LM, Chen CH, Yeh JI, Hsieh PS. 152.  et al. 2006. Association study of genetic polymorphisms of SLC2A10 gene and type 2 diabetes in the Taiwanese population. Diabetologia 49:1214–21 [Google Scholar]
  153. Guillam MT, Hummler E, Schaerer E, Yeh JI, Birnbaum MJ. 153.  et al. 1997. Early diabetes and abnormal postnatal pancreatic islet development in mice lacking Glut-2. Nat. Genet. 17:327–30 [Google Scholar]
  154. Manolescu AR, Augustin R, Moley K, Cheeseman C. 154.  2007. A highly conserved hydrophobic motif in the exofacial vestibule of fructose transporting SLC2A proteins acts as a critical determinant of their substrate selectivity. Mol. Membr. Biol. 24:455–63 [Google Scholar]
  155. Horikawa Y, Iwasaki N, Hara M, Furuta H, Hinokio Y. 155.  et al. 1997. Mutation in hepatocyte nuclear factor 1β gene (TCF2) associated with MODY. Nat. Genet. 17:384–85 [Google Scholar]
  156. Friedel S, Antwerpen B, Hoch A, Vogel C, Grassl W. 156.  et al. 2002. Glucose transporter 4 gene: association studies pertaining to alleles of two polymorphisms in extremely obese children and adolescents and in normal and underweight controls. Ann. N.Y. Acad. Sci. 967:554–57 [Google Scholar]
  157. Leney SE, Tavaré JM. 157.  2009. The molecular basis of insulin-stimulated glucose uptake: signalling, trafficking and potential drug targets. J. Endocrinol. 203:1–18 [Google Scholar]
  158. Kusari J, Verma US, Buse JB, Henry RR, Olefsky JM. 158.  1991. Analysis of the gene sequences of the insulin receptor and the insulin-sensitive glucose transporter (GLUT-4) in patients with common-type non-insulin-dependent diabetes mellitus. J. Clin. Investig. 88:1323–30 [Google Scholar]
  159. Katz EB, Stenbit AE, Hatton K, DePinho R, Charron MJ. 159.  1995. Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature 377:151–55 [Google Scholar]
  160. Kayano T, Burant CF, Fukumoto H, Gould GW, Fan YS. 160.  et al. 1990. Human facilitative glucose transporters. Isolation, functional characterization, and gene localization of cDNAs encoding an isoform (GLUT5) expressed in small intestine, kidney, muscle, and adipose tissue and an unusual glucose transporter pseudogene–like sequence (GLUT6). J. Biol. Chem. 265:13276–82 [Google Scholar]
  161. Burant CF, Takeda J, Brot-Laroche E, Bell GI, Davidson NO. 161.  1992. Fructose transporter in human spermatozoa and small intestine is GLUT5. J. Biol. Chem. 267:14523–26 [Google Scholar]
  162. Rand EB, Depaoli AM, Davidson NO, Bell GI, Burant CF. 162.  1993. Sequence, tissue distribution, and functional characterization of the rat fructose transporter GLUT5. Am. J. Physiol. Gastrointest. Liver Physiol. 264:G1169–76 [Google Scholar]
  163. Blakemore SJ, Aledo JC, James J, Campbell FC, Lucocq JM, Hundal HS. 163.  1995. The GLUT5 hexose transporter is also localized to the basolateral membrane of the human jejunum. Biochem. J. 309:7–12 [Google Scholar]
  164. Corpe CP, Bovelander FJ, Munoz CM, Hoekstra JH, Simpson IA. 164.  et al. 2002. Cloning and functional characterization of the mouse fructose transporter, GLUT5. Biochim. Biophys. Acta 1576:191–97 [Google Scholar]
  165. Wallace C, Newhouse SJ, Braund P, Zhang F, Tobin M. 165.  et al. 2008. Genome-wide association study identifies genes for biomarkers of cardiovascular disease: serum urate and dyslipidemia. Am. J. Hum. Genet. 82:139–49 [Google Scholar]
  166. Ghosh S, Watanabe RM, Hauser ER, Valle T, Magnuson VL. 166.  et al. 1999. Type 2 diabetes: evidence for linkage on chromosome 20 in 716 Finnish affected sib pairs. PNAS 96:2198–203 [Google Scholar]
  167. Watson RT, Pessin JE. 167.  2007. GLUT4 translocation: the last 200 nanometers. Cell Signal. 19:2209–17 [Google Scholar]
  168. Coucke PJ, Willaert A, Wessels MW, Callewaert B, Zoppi N. 168.  et al. 2006. Mutations in the facilitative glucose transporter GLUT10 alter angiogenesis and cause arterial tortuosity syndrome. Nat. Genet. 38:452–57 [Google Scholar]
  169. Doege H, Bocianski A, Scheepers A, Axer H, Eckel J. 169.  et al. 2001. Characterization of human glucose transporter (GLUT) 11 (encoded by SLC2A11), a novel sugar-transport facilitator specifically expressed in heart and skeletal muscle. Biochem. J. 359:443–49 [Google Scholar]
  170. Williams RSB, Cheng L, Mudge AW, Harwood AJ. 170.  2002. A common mechanism of action for three mood-stabilizing drugs. Nature 417:292–95 [Google Scholar]
  171. Di Daniel E, Cheng L, Maycox PR, Mudge AW. 171.  2006. The common inositol-reversible effect of mood stabilizers on neurons does not involve GSK3 inhibition, myo-inositol-1-phosphate synthase or the sodium-dependent myo-inositol transporters. Mol. Cell Neurosci. 32:27–36 [Google Scholar]
  172. Widmer M, Uldry M, Thorens B. 172.  2005. Glut8 subcellular localization and absence of translocation to the plasma membrane in PC12 cells and hippocampal neurons. Endocrinology 146:4727–36 [Google Scholar]
  173. Turk E, Zabel B, Mundlos S, Dyer J, Wright EM. 173.  1991. Glucose/galactose malabsorption caused by a defect in the Na+/glucose cotransporter. Nature 350:354–56 [Google Scholar]
  174. Xin B, Wang H. 174.  2011. Multiple sequence variations in SLC5A1 gene are associated with glucose-galactose malabsorption in a large cohort of Old Order Amish. Clin. Genet. 79:86–91 [Google Scholar]
  175. Van den Heuvel LP, Assink K, Willemsen M, Monnens L. 175.  2002. Autosomal recessive renal glucosuria attributable to a mutation in the sodium glucose cotransporter (SGLT2). Hum. Genet. 111:544–47 [Google Scholar]
  176. Yu L, Lv J-C, Zhou X, Zhu L, Hou P, Zhang H. 176.  2011. Abnormal expression and dysfunction of novel SGLT2 mutations identified in familial renal glucosuria patients. Hum. Genet. 129:335–44 [Google Scholar]
  177. Díez-Sampedro A, Hirayama BA, Osswald C, Gorboulev V, Baumgarten K. 177.  et al. 2003. A glucose sensor hiding in a family of transporters. PNAS 100:11753–58 [Google Scholar]
  178. Tazawa S, Yamato T, Fujikura H, Hiratochi M, Itoh F. 178.  et al. 2005. SLC5A9/SGLT4, a new Na+-dependent glucose transporter, is an essential transporter for mannose, 1,5-anhydro-d-glucitol, and fructose. Life Sci. 76:1039–50 [Google Scholar]
  179. Ghezzi C, Gorraitz E, Hirayama BA, Loo DD, Grempler R. 179.  et al. 2014. Fingerprints of hSGLT5 sugar and cation selectivity. Am. J. Physiol. Cell Physiol. 308:C864–70 [Google Scholar]
  180. Gorboulev V, Schürmann A, Vallon V, Kipp H, Jaschke A. 180.  et al. 2012. Na+-d-glucose cotransporter SGLT1 is pivotal for intestinal glucose absorption and glucose-dependent incretin secretion. Diabetes 61:187–96 [Google Scholar]
  181. Vallon V, Platt KA, Cunard R, Schroth J, Whaley J. 181.  et al. 2011. SGLT2 mediates glucose reabsorption in the early proximal tubule. J. Am. Soc. Nephrol. 22:104–12 [Google Scholar]
  182. Engel ML, Holmes-Davis R, McCormick S. 182.  2005. Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol. 138:2124–33 [Google Scholar]
  183. Lee J, Lee H, Kim J, Lee S, Kim DH. 183.  et al. 2011. Both the hydrophobicity and a positively charged region flanking the C-terminal region of the transmembrane domain of signal-anchored proteins play critical roles in determining their targeting specificity to the endoplasmic reticulum or endosymbiotic organelles in arabidopsis cells. Plant Cell 23:1588–607 [Google Scholar]
  184. Seo PJ, Park JM, Kang SK, Kim SG, Park CM. 184.  2011. An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233:189–200 [Google Scholar]
/content/journals/10.1146/annurev-biochem-060614-033904
Loading
/content/journals/10.1146/annurev-biochem-060614-033904
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • 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