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Review

Structure of, and functional insight into the GLUT family of membrane transporters

&
Pages 167-183 | Published online: 06 Oct 2015

References

  • Brett KE, Ferraro ZM, Holcik M, Adamo KB. Prenatal physical activity and diet composition affect the expression of nutrient transporters and mTOR signaling molecules in the human placenta. Placenta. 2015;36:204–212.
  • Hedicer A, Budarf ML, Emanuel BS, Mohandas TK, Wright EM. Assignment of the human intestinal Na+/glucose cotransporter transporter. Genomics. 1989;4:297–300.
  • Wright EM, Turk E, Hager K, et al. The Na+/glucose cotransporter (SGLT1). Acta Physiol Scand Suppl. 1992;607:201–207.
  • Pao SS, Paulsen IT, Saier MH. Major facilitator superfamily. Microbiol Mol Biol Rev. 1998;62:1–34.
  • Saier MH, Beatty JT, Goffeau A, et al. The major facilitator superfamily. J Mol Microbiol Biotechnol. 1999;1:257–279.
  • Cura AJ, Carruthers AJ. The role of monosaccharide transport proteins in carbohydrate assimilation, distribution, metabolism and homeostasis. Compr Physiol. 2013;2:863–914.
  • Manolescu AR, Witkowska K, Kinnaird A, Cessford T, Cheeseman C. Facilitated hexose transporters: new perspectives on form and function. Physiology. 2007;22:234–240.
  • Thorens B, Mueckler M. Glucose transporters in the 21st century. Am J Physiol Endocrinol Metab. 2010;298:141–145.
  • Kasahara M, Hinkle PC. Reconstitution and purification of the D-glucose transporter from human erythrocytes. J Biol Chem. 1977;252:7384–7390.
  • Sogin DC, Hinkle PC. Characterization of the glucose transporter from human erythrocytes. J Supramol Struct. 1978;8:447–453.
  • Mueckler M, Caruso C, Baldwin SA, et al. Sequence and structure of a human glucose transporter. Science. 1985;229:941–945.
  • Thorens B, Sarkar HK, Kaback HR, Lodish HF. Cloning and functional expression in bacteria of a novel glucose transporter present in liver, intestine, kidney, and beta-pancreatic islet cells. Cell. 1988;55:281–290.
  • Fukumoto H, Kayano T, Buse JB, et al. Cloning and characterization of the major insulin-responsive glucose transporter expressed in human skeletal muscle and other insulin-responsive tissues. J Biol Chem. 1989;264:7776–7779.
  • Cheeseman CI. GLUT2 is the transporter for fructose across the rat intestinal basolateral membrane. Gastroenterology. 1993;105:1050–1056.
  • Colville CA, Seatter MJ, Jess TJ, Gould GW, Thomas HM. Kinetic analysis of the liver-type (GLUT2) and brain-type (GLUT3) glucose transporters in Xenopus oocytes: substrate specificities and effects of transport inhibitors. Biochem J. 1993;290 Pt 3:701–706.
  • Craik JD, Elliott KR. Kinetics of 3-O-methyl-D-glucose transport in isolated rat hepatocytes. Biochem J. 1979;182:503–508.
  • Kayanos T, Fukumotoo H, Eddyl RL, et al. Evidence for a family of human glucose transporter-like proteins. Biol Chem. 1988;263:15245–15248.
  • Yano H, Seino Y, Inagaki N, et al. Tissue distribution and species difference of the brain type glucose transporter (GLUT3). Biochem Biophys Res Commun. 1991;174:470–477.
  • Shepherd PR, Gould GW, Colville CA, McCoid SC, Gibbs EM, Kahn BB. Distribution of GLUT3 glucose transporter protein in human tissues. Biochem Biophys Res Commun. 1992;188:149–154.
  • Wu, X, Freeze HH. GLUT14, a duplicon of GLUT3, is specially expressed in testis as alternative splice forms. Genomics. 2002;80:553–557.
  • Clancy BM, Czech MP. Hexose transport stimulation and membrane redistribution of glucose transporter isoforms in response to cholera toxin, dibutyryl cyclic AMP, and insulin in 3T3-L1 adipocytes. J Biol Chem. 1990;265:12434–12443.
  • Kayano T, Burant CF, Fukumoto H, et al. 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. J Biol Chem. 1990;265:13276–13282.
  • Corpe CP, Basaleh MM, Affleck J, Gould G, Jess TJ, Kellett GL. The regulation of GLUT5 and GLUT2 activity in the adaptation of intestinal brush-border fructose transport in diabetes. Pflugers Arch. 1996;432:192–201.
  • Waddell ID, Zomerschoe AG, Voice MW, Burchell A. Cloning and expression of a hepatic microsomal glucose transport protein. Comparison with liver plasma-membrane glucose-transport protein GLUT 2. Biochem J. 1992;286 Pt 1:173–177.
  • Burchell A. A re-evaluation of GLUT 7. Biochem J. 1998;331 Pt 3:973.
  • Li Q, Manolescu A, Ritzel M, et al. Cloning and functional characterization of the human GLUT7 isoform SLC2A7 from the small intestine. Am J Physiol Gastrointest Liver Physiol. 2004;287:G236–G242.
  • Phay JE, Hussain HB, Moley JF. Cloning and expression analysis of a novel member of the facilitative glucose transporter family, SLC2A9 (GLUT9). Genomics. 2000;9:217–220.
  • Kimura T, Takahashi M, Yan K, Sakurai H. Expression of SLC2A9 isoforms in the kidney and their localization in polarized epithelial cells. PLoS One. 2014;9:e84996.
  • Caulfield MJ, Munroe PB, O’Neill D, et al. SLC2A9 is a high-capacity urate transporter in humans. PLoS Med. 2008;5:1509–1523.
  • Doege H, Bocianski A, Joost HG, Schürmann A. Activity and genomic organization of human glucose transporter 9 (GLUT9), a novel member of the family of sugar-transport facilitators predominantly expressed in brain and leucocytes. Biochem J. 2000;350 Pt 3:771–776.
  • Lisinski I, Schürmann A, Joost HG, Cushman SW, Al-Hasani H. Targeting of GLUT6 (formerly GLUT9) and GLUT8 in rat adipose cells. Biochem J. 2001;358:517–522.
  • Vitart V, Rudan I, Hayward C, et al. SLC2A9 is a newly identified urate transporter influencing serum urate concentration, urate excretion and gout. Nat Genet. 2008;40:437–442.
  • Doege H, Bocianski A, Scheepers A, et al. Characterization of human glucose transporter (GLUT) 11 (encoded by SLC2A11), a novel sugar-transport facilitator specifically expressed in heart and skeletal muscle. Biochem J. 2001;359:443–449.
  • Doege H, Schürmann A, Bahrenberg G, Brauers A, Joost HG. GLUT8, a novel member of the sugar transport facilitator family with glucose transport activity. J Biol Chem. 2000;275:16275–16280.
  • Ibberson M, Uldry M, Thorens B. GLUTX1, a novel mammalian glucose transporter expressed in the central nervous system and insulin-sensitive tissues. J Biol Chem. 2000;275:4607–4612.
  • McVie-Wylie AJ, Lamson DR, Chen YT. Molecular cloning of a novel member of the GLUT family of transporters, SLC2a10 (GLUT10), localized on chromosome 20q13.1: a candidate gene for NIDDM susceptibility. Genomics. 2001;72:113–117.
  • Dawson PA, Mychaleckyj JC, Fossey SC, Mihic SJ, Craddock AL, Bowden DW. Sequence and functional analysis of GLUT10: a glucose transporter in the type 2 diabetes-linked region of chromosome 20q12–13.1. Mol Genet Metab. 2001;74:186–199.
  • Rogers S, Macheda M, Docherty S, et al. Identification of a novel glucose transporter-like protein GLUT-12. Appl Phys Endocrinol Metab. 2002;283:E733–E738.
  • Wilson-O’Brien AL, DeHaan CL, Rogers S. Mitogen-stimulated and rapamycin-sensitive glucose transporter 12 targeting and functional glucose transport in renal epithelial cells. Endocrinology. 2008;149:917–924.
  • Razeghi P, Young ME, Alcorn JL, Moravec CS, Frazier OH, Taegtmeyer H. Metabolic gene expression in fetal and failing human heart. Circulation. 2001;104:2923–2931.
  • Rogers S, Docherty SE, Slavin JL, Henderson MA, Best JD. Differential expression of GLUT12 in breast cancer and normal breast tissue. Cancer Lett. 2003;193:225–233.
  • Gude NM, Stevenson JL, Rogers S, et al. GLUT12 expression in human placenta in first trimester and term. Placenta. 2003;24:566–570.
  • Rogers S, Chandler JD, Clarke AL, Petrou S, Best JD. Glucose transporter GLUT12-functional characterization in Xenopus laevis oocytes. Biochem Biophys Res Commun. 2003;308:422–426.
  • Uldry M, Ibberson M, Horisberger JD, Chatton JY, Riederer BM, Thorens B. Identification of a mammalian H+-myo-inositol symporter expressed predominantly in the brain. EMBO J. 2001;20:4467–4477.
  • Hresko RC, Kruse M, Strube M, Mueckler M. Topology of the GLUT1 glucose transporter deduced from glycosylation scanning mutagenesis. J Biol Chem. 1994;269:20482–20488.
  • Mueckler M. Facilitative glucose transporters. Eur J Biochem. 1994; 219: 713–725.
  • Cairns MT, Alvarez J, Panico M, et al. Investigation of the structure and function of the human erythrocyte glucose transporter by proteolytic dissection. Biochim Biophys Acta. 1987;905:295–310.
  • Zhao F-Q, Keating AF. Functional properties and genomics of glucose transporters. Curr Genomics. 2007;8:113–128.
  • Mori H, Hashiramoto M, Clark AE, et al. Substitution of tyrosine 293 of GLUT1 locks the transporter into an outward facing conformation. J Biol Chem. 1994;269:11578–11583.
  • Moris H, Muraokas A. Substitution at Pro385 of GLUTl perturbs the glucose transport function by reducing conformational flexibility. J Biol Chem. 1994;269:2982–2986.
  • Schürmann A, Doege H, Ohnimus H, Monser V, Buchs A, Joost HG. Role of conserved arginine and glutamate residues on the cytosolic surface of glucose transporters for transporter function. Biochemistry. 1997;36:12897–12902.
  • Olson AL, Pessin JE. Structure, function, and regulation of the mammalian facilitative glucose transporter gene family. Annu Rev Nutr. 1996;16:235–256.
  • Mueckler M, Weng W, Kruse M. Glutamine 161 of GLUT1 glucose transporter is critical for transport activity and exofacial ligand binding. J Biol Chem. 1994;269:20533–20538.
  • Doege H, Schürmann A, Ohnimus H, Monser V, Holman GD, Joost HG. Serine-294 and threonine-295 in the exofacial loop domain between helices 7 and 8 of glucose transporters (GLUT) are involved in the conformational alterations during the transport process. Biochem J. 1998;329 Pt 2:289–293.
  • Garcia JC, Strube M, Leingang K, Keller K, Mueckler MM. Amino acid substitutions at tryptophan 388 and tryptophan 412 of the HepG2 (Glut1) glucose transporter inhibit transport activity and targeting to the plasma membrane in Xenopus oocytes. J Biol Chem. 1992;267:7770–7776.
  • Schürmann A, Keller K, Monden I, et al. Glucose transport activity and photolabelling with 3-[125I]iodo-4-azidophenethylamido-7-O-succinyldeacetyl (IAPS)-forskolin of two mutants at tryptophan-388 and -412 of the glucose transporter GLUT1: dissociation of the binding domains of forskolin and glucose. Biochem J. 1993;290 Pt 2:497–501.
  • Seatter MJ, De La Rue SA, Porter LM, Gould GW. QLS motif in transmembrane helix VII of the glucose transporter family interacts with the C-1 position of D-glucose and is involved in substrate selection at the exofacial binding site. Biochemistry. 1998;37:1322–1326.
  • Joost H, Thorens B. The extended GLUT-family of sugar/polyol transport facilitators: nomenclature, sequence characteristics, and potential function of its novel members. Mol Membr Biol. 2001;18:257–264.
  • Manolescu AR, Augustin R, Moley K, Cheeseman C. 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. 2007;24:455–463.
  • Manolescu A, Salas-Burgos AM, Fischbarg J, Cheeseman CI. Identification of a hydrophobic residue as a key determinant of fructose transport by the facilitative hexose transporter SLC2A7 (GLUT7). J Biol Chem. 2005;280:42978–42983.
  • Long W, Panwar P, Witkowska K, et al. Critical roles of two hydrophobic residues within human glucose transporter 9 (hSLC2A9) in substrate selectivity and urate transport. J Biol Chem. 2015;290:15292–15303.
  • Alvarez J, Lee DC, Baldwin SA, Chapman D. Fourier transform infrared spectroscopic study of the structure and conformational changes of the human erythrocyte glucose transporter. J Biol Chem. 1987;262:3502–3509.
  • Chin JJ, Jung EK, Chen V, Jung CY. Structural basis of human erythrocyte glucose transporter function in proteoliposome vesicles: circular dichroism measurements. Proc Natl Acad Sci U S A. 1987;84:4113–4116.
  • Heinze M, Monden I, Keller K. Cysteine-scanning mutagenesis of transmembrane segment 1 of glucose transporter GLUT1: extracellular accessibility of helix positions. Biochemistry. 2004;43:931–936.
  • Mueckler M, Roach W, Makepeace C. Transmembrane segment 3 of the GLUT1 glucose transporter is an outer helix. J Biol Chem. 2004;279:46876–46881.
  • Mueckler M, Makepeace C. Cysteine-scanning mutagenesis and substituted cysteine accessibility analysis of transmembrane segment 4 of the GLUT1 glucose transporter. J Biol Chem. 2005;280:39562–39568.
  • Mueckler M, Makepeace C. Transmembrane segment 5 of the Glut1 glucose transporter is an amphipathic helix that forms part of the sugar permeation pathway. J Biol Chem. 1999;274:10923–10926.
  • Mueckler M, Makepeace C. Transmembrane segment 6 of the Glut1 glucose transporter is an outer helix and contains amino acid side chains essential for transport activity. J Biol Chem. 2008;283:11550–11555.
  • Hruz PW, Mueckler MM. Cysteine-scanning mutagenesis of transmembrane segment 7 of the GLUT1 glucose transporter. J Biol Chem. 1999;274:36176–36180.
  • Mueckler M, Makepeace C. Model of the exofacial substrate-binding site and helical folding of the human Glut1 glucose transporter based on scanning mutagenesis. Biochemistry. 2009;48:5934–5942.
  • Hruz PW, Mueckler MM. Cysteine-scanning mutagenesis of transmembrane segment 11 of the GLUT1 facilitative glucose transporter. Biochemistry. 2000;39(51):9367–9372.
  • Mueckler M, Makepeace C. Transmembrane segment 12 of the Glut1 glucose transporter is an outer helix and is not directly involved in the transport mechanism. J Biol Chem. 2006;281(48):36993–36998.
  • Mueckler M, Makepeace C. Analysis of Transmembrane Segment 8 of the GLUT1 Glucose Transporter by Cysteine-scanning Mutagenesis and Substituted Cysteine Accessibility. J Biol Chem. 2003;279:10494–10499.
  • Mueckler M, Makepeace C. Analysis of transmembrane segment 10 of the Glut1 glucose transporter by cysteine scanning mutagenesis and substituted cysteine accessibility. J Biol Chem. 2002;277(5):3498–3503.
  • Salas-Burgos A, Iserovich P, Zuniga F, Vera JC, Fischbarg J. Predicting the three-dimensional structure of the human facilitative glucose transporter GLUT1 by a novel evolutionary homology strategy: insights on the molecular mechanism of substrate migration, and binding sites for glucose and inhibitory molecules. Biophys J. 2004;87:2990–2999.
  • Saier MH. Phylogenetic approaches to the identification and characterization of protein families and superfamilies. Microb Comp Genomics. 1996;1:129–150.
  • Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S. Structure and mechanism of the lactose permease of Escherichia coli. Science. 2003;301:610–615.
  • Lemieux MJ. Eukaryotic major facilitator superfamily transporter modeling based on the prokaryotic GlpT crystal structure. Mol Membr Biol. 2007;24:333–341.
  • Dwyer DS. Model of the 3-D structure of the GLUT3 glucose transporter and molecular dynamics simulation of glucose transport. Proteins. 2001;42:531–541.
  • Mohan SS, Perry JJ, Poulose N, Nair BG, Anilkumar G. Homology modeling of GLUT4, an insulin regulated facilitated glucose transporter and docking studies with ATP and its inhibitors. J Biomol Struct Dyn. 2009;26:455–464.
  • Madej MG, Sun L, Yan N, Kaback HR. Functional architecture of MFS D-glucose transporters. Proc Natl Acad Sci U S A. 2014;111: E719–E727.
  • Clémençon B, Lüscher BP, Fine M, et al. Expression, purification, and structural insights for the human uric acid transporter, GLUT9, using the Xenopus laevis oocytes system. PLoS One. 2014;9:e108852.
  • Chang G, Spencer RH, Lee AT, Barclay MT, Rees DC. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science. 1998;282:2220–2226.
  • Deng D, Xu C, Sun P, et al. Crystal structure of the human glucose transporter GLUT1. Nature. 2014;510:121–125.
  • Sun L, Zeng X, Yan C, et al. Crystal structure of a bacterial homologue of glucose transporters GLUT1–4. Nature. 2012;490:361–366.
  • Iancu CV, Zamoon J, Woo SB, Aleshin A, Choe JY. Crystal structure of a glucose/H+ symporter and its mechanism of action. Proc Natl Acad Sci U S A. 2013;110:17862–17867.
  • Deng D, Sun P, Yan C, et al. Molecular basis of ligand recognition and transport by glucose transporters. Nature. July 15, 2015. doi:10.1038/nature14655.
  • Widdas W. Inability of diffusion to account for placental glucose transfer in the sheep and consideration of the kinetics of a possible carrier transfer. J Physiol. 1952;118:23–39.
  • Fisher RB, Parsons DS. Glucose movements across the wall of the rat small intestine. J Physiol. 1953;119:210–223.
  • Fisher RB, Parsons DS. Galatose absorption from the surviving small intestine of the rat. J Physiol. 1953;119:224–232.
  • Neame KD, Richards TG, editors. Elementary Kinetics of Membrane Carrier Transport. 1st ed. London, UK: Blackwell Scientific Publications; 1972.
  • Naftalin RJ, Holman GD. Transport of sugars in human red cells. In: Ellory JC, Lew V, editors. Membrane Transport in Red Cells. New York, NY, USA: Academic Press; 1977.
  • Regen DM, Tarpley HL. Anomalous transport kinetics and the glucose carrier hypothesis. Biochim Biophys Acta. 1974;339:218–233.
  • Eilam Y. Two-carrier models for mediated transport. 1. Theoretical analysis of several two-carrier models. Biochim Biophys Acta. 1975; 401: 349–363.
  • Naftalin RJ. Model for sugar transport across red cell membrane without carriers. Biochim Biophys Acta. 1970;211:65–78.
  • Lieb WR, Stein WD. Quantitative predictions of a noncarrier model for glucose transport across the human red cell membrane. Biophys J. 1970;10:585–609.
  • LeFevre PG. A model for erythrocyte sugar transport based on substrate-conditioned “introversion” of binding sites. J Membr Biol. 1973;11:1–19.
  • Mueckler M, Thorens B. The SLC2 (GLUT) family of membrane transporters. Mol Asp Med. 2013;34:121–138.
  • Naftalin RJ. Alternating carrier models of asymmetric glucose transport violate the energy conservation laws. Biophys J. 2008;95:4300–4314.
  • Vollers SS, Carruthers A. Sequence determinants of GLUT1-mediated accelerated-exchange transport: analysis by homology-scanning mutagenesis. J Biol Chem. 2012;287:42533–42544.
  • Carruthers A, DeZutter J, Ganguly A, Devaskar SU. Will the original glucose transporter isoform please stand up! Am J Physiol Endocrinol Metab. 2009;297:E836–E848.
  • Toyoda N, Flanagan JE, Kono T. Reassessment of insulin effects on the V(max) and K(m) values of hexose transport in isolated rat epididymal adipocytes. J Biol Chem. 1987;262:2737–2745.
  • Taylor LP, Holman GD. Symmetrical kinetic parameters for 3-O-methyl-D-glucose transport in adipocytes in the presence and in the absence of insulin. Biochim Biophys Acta. 1981;642:325–335.
  • Pessino A, Hebert DN, Woon CW, et al. Evidence that functional erythrocyte-type glucose transporters are oligomers. J Biol Chem. 1991;266:20213–20217.
  • Zottola RJ, Cloherty EK, Coderre PE, Hansen A, Hebert DN, Carruthers A. Glucose transporter function is controlled by transporter oligomeric structure. A single, intramolecular disulfide promotes GLUT1 tetramerization. Biochemistry. 1995;34:9734–9747.
  • Cloherty EK, Levine KB, Carruthers A. The red blood cell glucose transporter presents multiple, nucleotide-sensitive sugar exit sites. Biochemistry. 2001;40:15549–15561.
  • De Zutter JK, Levine KB, Deng D, Carruthers A. Sequence determinants of GLUT1 oligomerization: analysis by homology-scanning mutagenesis. J Biol Chem. 2013;288:20734–20744.
  • Lemieux MJ, Huang Y, Wang da N. Crystal structure and mechanism of GlpT, the glycerol-3-phosphate transporter from E. coli. J Electron Microsc (Tokyo). 2005;54 Suppl 1:43–46.
  • Dang S, Sun L, Huang Y, et al. Structure of a fucose transporter in an outward-open conformation. Nature. 2010;467:734–738.
  • Jardetzky O. Simple allosteric model for membrane pumps. Nature. 1966;211:969–970.
  • Park CR, Crofford OB, Kono T. Mediated (nonactive) transport of glucose in mammalian cells and its regulation. J Gen Physiol. 1968;52:296–318.
  • Rosenberg T, Wilbrandt W. Uphill transport induced by counterflow. J Gen Physiol. 1957;41:289–296.
  • Maher F, Davies-Hill TM, Simpson IA. Substrate specificity and kinetic parameters of GLUT3 in rat cerebellar granule neurons. J Biol Chem. 1996;315:827–831.
  • Liu Q, Vera JC, Peng H, Golde DW. The predicted ATP-binding domains in the hexose transporter GLUT1 critically affect transporter activity. Biochemistry. 2001;40:7874–7881.
  • Sweet IR, Matschinsky FM. Are there kinetic advantages of GLUT2 in pancreatic glucose sensing? Diabetologia. 1997;40:112–119.
  • Clark AE, Holman GD, Kozka IJ. Determination of the rates of appearance and loss of glucose transporters at the cell surface of rat adipose cells. Biochem J. 1991;278 Pt 1:235–241.
  • Haney PM, Slot JW, Piper RC, James DE, Mueckler M. Intracellular targeting of the insulin-regulatable glucose transporter (GLUT4) is isoform specific and independent of cell type. J Cell Biol. 1991;114:689–699.
  • Hudson AW, Ruiz M, Birnbaum MJ. Isoform-specific subcellular targeting of glucose transporters in mouse fibroblasts. J Cell Biol. 1992;116:785–797.
  • Hudson AW, Fingar DC, Seidner GA, Griffiths G, Burke B, Birnbaum MJ. Targeting of the “insulin-responsive” glucose transporter (GLUT4) to the regulated secretory pathway in PC12 cells. J Cell Biol. 1993;122:579–588.
  • Piper RC, Tai C, Slot JW, et al. The efficient intracellular sequestration of the insulin-regulatable glucose transporter (GLUT-4) is conferred by the NH2 terminus. J Cell Biol. 1992;117:729–743.
  • Shibasaki Y, Asano T, Lin JL, et al. Two glucose transporter isoforms are sorted differentially and are expressed in distinct cellular compartments. Biochem J. 1992;281 Pt 3:829–834.
  • Verhey KJ, Hausdorff SF, Birnbaum MJ. Identification of the carboxy terminus as important for the isoform-specific subcellular targeting of glucose transporter proteins. J Cell Biol. 1993;123:137–147.
  • Riskin A, Nannegari VH, Mond Y. Acute effectors of GLUT1 glucose transporter subcellular targeting in CIT3 mouse mammary epithelial cells. Pediatr Res. 2008;63:56–61.
  • Czech MP, Chawla A, Woon CW, et al. Exofacial epitope-tagged glucose transporter chimeras reveal COOH-terminal sequences governing cellular localization. J Cell Biol. 1993;123:127–135.
  • Andrisse S, Patel GD, Chen JE, et al. ATM and GLUT1-S490 phosphorylation regulate GLUT1 mediated transport in skeletal muscle. PLoS One. 2013;8:e66027.
  • Inukai K, Shewan AM, Pascoe WS, Katayama S, James DE, Oka Y. Carboxy terminus of glucose transporter 3 contains an apical membrane targeting domain. Mol Endocrinol. 2004;18:339–349.
  • Yang J, Holman GD. Comparison of GLUT4 and GLUT1 subcellular trafficking in basal and insulin-stimulated 3T3-L1 cells. J Biol Chem. 1993;268:4600–4603.
  • Yang J, Clark AE, Harrison R, Kozka IJ, Holman GD. Trafficking of glucose transporters in 3T3-L1 cells trafficking proteins. 1992;281:809–817.
  • Egert S, Nguyen N, Schwaiger M. Myocardial glucose transporter GLUT1: translocation induced by insulin and ischemia. J Mol Cell Cardiol. 1999;31:1337–1344.
  • El-Jack AK, Kandror KV, Pilch PF. The formation of an insulin-responsive vesicular cargo compartment is an early event in 3T3-L1 adipocyte differentiation. Mol Biol Cell. 1999;10:1581–1594.
  • Mueckler M. The molecular biology of mammalian glucose transporters. Curr Opin Nephrol Hypertens. 1992;1:12–20.
  • Roach W, Plomann M. PACSIN3 overexpression increases adipocyte glucose transport through GLUT1. Biochem Biophys Res Commun. 2007;355:745–750.
  • Nakayama T, Kamiguchi H, Akagawa K. Syntaxin 1C, a soluble form of syntaxin, attenuates membrane recycling by destabilizing microtubules. J Cell Sci. 2012;125:817–830.
  • Cura AJ, Carruthers A. AMP kinase regulation of sugar transport in brain capillary endothelial cells during acute metabolic stress. Am J Physiol Cell Physiol. 2012;303:C806–C814.
  • Caliceti C, Zambonin L, Prata C, et al. Effect of plasma membrane cholesterol depletion on glucose transport regulation in leukemia cells. PLoS One. 2012;7:e41246.
  • Fang J, Zhou SH, Fan J, Yan SX. Roles of glucose transporter-1 and the phosphatidylinositol 3-kinase/protein kinase B pathway in cancer radioresistance. Mol Med Rep. 2015;11:1573–1578.
  • Wofford JA, Wieman HL, Jacobs SR, Zhao Y, Rathmell JC, Jeffrey C. IL-7 promotes Glut1 trafficking and glucose uptake via STAT5-mediated activation of Akt to support T cell survival. Blood. 2008;111:2101–2112.
  • Zambrano A, Jara E, Murgas P, et al. Cytokine stimulation promotes increased glucose uptake via translocation at the plasma membrane of GLUT1 in HEK293 cells. J Cell Biochem. 2010;110:1471–1480.
  • Sommermann TG, O’Neill K, Plas DR, Cahir-McFarland E. IKK² and NF-ºB transcription govern lymphoma cell survival through AKT-induced plasma membrane trafficking of GLUT1. Cancer Res. 2011;71:7291–7300.
  • Stockli J, Fazakerley DJ, James DE. GLUT4 exocytosis. J Cell Sci. 2011;124:4147–4159.
  • Belman JP, Habtemichael EN, Bogan JS. A proteolytic pathway that controls glucose uptake in fat and muscle. Rev Endocr Metab Disord. 2014;15:55–66.
  • Alvim RO, Cheuhen MR, Machado SR. General aspects of muscle glucose uptake. 2015;87:351–368.
  • Cushman SW, Wardzala LJ. Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. Apparent translocation of intracellular transport systems to the plasma membrane. J Biol Chem. 1980;255(10):4758–4762.
  • Millar CA, Powell KA, Hickson GR, Bader MF, Gould GW. Evidence for a role for ADP-ribosylation factor 6 in insulin-stimulated glucose transporter-4 (GLUT4) trafficking in 3T3-L1 adipocytes. J Biol Chem. 1999;274:17619–17625.
  • van Dam EM, Govers R, James DE. Akt activation is required at a late stage of insulin-induced GLUT4 translocation to the plasma membrane. Mol Endocrinol. 2005;19:1067–1077.
  • Backer JM, Myers MG, Shoelson SE, et al. Phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 1992;11:3469–3479.
  • White MF, Kahn CR. The insulin signaling system. J Biol Chem. 1994;269:1–4.
  • Zorzano A, Munoz P, Camps M, Mora C, Testar X, Palacin M. Insulin-induced redistribution of GLUT4 glucose carriers in the muscle fiber: in search of GLUT4 trafficking pathways. Diabetes. 1996;45 Suppl 1: S70–S81.
  • Steinbusch LK, Schwenk RW, Ouwens DM, Diamant M, Glatz JF, Luiken JJ. Subcellular trafficking of the substrate transporters GLUT4 and CD36 in cardiomyocytes. Cell Mol Life Sci. 2011;68:2525–2538.
  • Capilla E, Suzuki N, Pessin JE, Hou JC. The glucose transporter 4 FQQI motif is necessary for Akt substrate of 160-kilodalton-dependent plasma membrane translocation but not Golgi-localized (gamma)-ear-containing Arf-binding protein-dependent entry into the insulin-responsive storage compartment. Mol Endocrinol. 2007;21:3087–3099.
  • Khan AH, Capilla E, Hou JC, Watson RT, Smith JE, Pessin JE. Entry of newly synthesized GLUT4 into the insulin-responsive storage compartment is dependent upon both the amino terminus and the large cytoplasmic loop. J Biol Chem. 2004;279:37505–37511.
  • Tsuchiya A, Kanno T, Nishizaki T. Diacylglycerol promotes GLUT4 translocation to the cell surface in a PKCµ-dependent and PKC»/¹ and -¶- independent manner. Life Sci. 2013;93:240–246.
  • Asano T, Kanda A, Katagiri H, et al. P110² is up-regulated during differentiation of 3T3-L1 cells and contributes to the highly insulin-responsive glucose transport activity. J Biol Chem. 2000;275:17671–17676.
  • Waller A, Kohler K, Burns T, Mudge M, Belknap J, Lacombe V. Naturally- occurring compensated insulin resistance selectively alters glucose transporters in visceral and subcutaneous adipose tissue without change in AS 160 activation. Biochim Biophys Acta. 2011;1812:1098–1103.
  • Tsuchiya Y, Hatakeyama H, Emoto N, Wagatsuma F, Matsushita S, Kanzaki M. Palmitate-induced down-regulation of sortilin and impaired GLUT4 trafficking in C2C12 myotubes. J Biol Chem. 2010;285:34371–34381.
  • Hong YH, Betik AC, McConell GK. Role of nitric oxide in skeletal muscle glucose uptake during exercise. Exp Physiol. 2014;99:1569–1573.
  • Li Q, Zhu X, Ishikura S, et al. Ca2+ signals promote GLUT4 exocytosis and reduce its endocytosis in muscle cells. Am J Physiol Endocrinol Metab. 2014;307:e209–e224.
  • Kellett GL, Helliwell PA. The diffusive component of intestinal glucose absorption is mediated by the glucose-induced recruitment of GLUT2 to the brush-border membrane. Biochem J. 2000;350:155–162.
  • Tobin V, Le Gall M, Fioramonti X, et al. Insulin internalizes GLUT2 in the enterocytes of healthy but not insulin-resistant mice. Diabetes. 2008;57:555–562.
  • Helliwell P, Richardson M, Affleck J, Kellett G. Stimulation of fructose transport across the intestinal brush-border membrane by PMA is mediated by GLUT2 and dynamically regulated by protein kinase C. Biochem J. 2000;350:149–154.
  • Mace OJ, Lister N, Morgan E, et al. An energy supply network of nutrient absorption coordinated by calcium and T1R taste receptors in rat small intestine. J Physiol. 2009;587 Pt 1:195–210.
  • Cheeseman CI, O’Neill D. Basolateral D-glucose transport activity along the crypt-villus axis in rat jejunum and upregulation induced by gastric inhibitory peptide and glucagon-like peptide-2. Exp Physiol. 1998;83:605–616.
  • Shepherd EJ, Helliwell PA, Mace OJ, Morgan EL, Patel N, Kellett GL. Stress and glucocorticoid inhibit apical GLUT2-trafficking and intestinal glucose absorption in rat small intestine. J Physiol. 2004;560 Pt 1: 281–290.
  • Habold C, Foltzer-Jourdainne C, Le Maho Y, Lignot J-H, Oudart H. Intestinal gluconeogenesis and glucose transport according to body fuel availability in rats. J Physiol. 2005;566 Pt 2:575–586.
  • Wis´niewski J, Friedrich A, Keller T, Mann M, Koepsell H. The impact of high-fat diet on metabolism and immune defense in small intestine mucosa. J Proteome Res. 2015;14:353–365.
  • Cohen M, Kitsberg D, Tsytkin S, Shulman M, Aroeti B, Nahmias Y. Live imaging of GLUT2 glucose-dependent trafficking and its inhibition in polarized epithelial cysts. Open Biol. 2014;4:140091.
  • Greenlee W, Heather M, Uemura E, Carpenter SL, Doyle RT, Buss JE. Glucose uptake in PC12 cells: GLUT3 vesicle trafficking and fusion as revealed with a novel GLUT3-GFP fusion protein. J Neurosci Res. 2003;73:518–525.
  • McClory H, Williams D, Sapp E, et al. Glucose transporter 3 is a rab11-dependent trafficking cargo and its transport to the cell surface is reduced in neurons of CAG140 Huntington’s disease mice. Acta Neuropathol Commun. 2014;2:1–9.
  • Pinto AB, Carayannopoulos MO, Hoehn A, Dowd L, Moley KH. Glucose transporter 8 expression and translocation are critical for murine blastocyst survival. Biol Reprod. 2002;66:1729–1733.
  • Carayannopoulos MO, Chi MM, Cui Y, et al. GLUT8 is a glucose transporter responsible for insulin-stimulated glucose uptake in the blastocyst. Proc Natl Acad Sci U S A. 2000;97:7313–7318.
  • Wyman AH, Chi M, Riley J, et al. Syntaxin 4 expression affects glucose transporter 8 translocation and embryo survival. Mol Endocrinol. 2003;17:2096–2102.
  • Piroli GG, Grillo CA, Hoskin EK, et al. Peripheral glucose administration stimulates the translocation of GLUT8 glucose transporter to the endoplasmic reticulum in the rat hippocampus. J Comp Neurol. 2002;452:103–114.
  • Augustin R, Riley J, Moley KH. GLUT8 contains [DE]XXXL[LI] sorting motif and localizes to a late endomosal/lysosomal compartment. Traffic. 2005;6:1196–1212.
  • Flessner L, Moley K. Similar [DE]XXX[LI] motif differentially target GLUT8 and GLUT12 in Chinese hamster ovary cells. Traffic. 2010;10:324–333.
  • Piroli GG, Grillo C a., Hoskin EK, et al. Peripheral glucose administration stimulates the translocation of GLUT8 glucose transporter to the endoplasmic reticulum in the rat hippocampus. J Comp Neurol. 2002;452(2):103–114.
  • Aerni-Flessner L, Otu M, Moley K. The amino acids upstream of NH(2)-terminal dileucine motif play a role in regulating the intracellular sorting of the Class III transporters GLUT8 and GLUT12. Mol Membr Biol. 2011;28:30–41.
  • De Vivo DC, Trifiletti RR, Jacobson RI, Ronen GM, Behmand RA, Harik SI. Defective glucose transport across the blood-brain barrier as a cause of persistent hypoglycorrhachia, seizures, and development delay. N Engl J Med. 1991;325:703–709.
  • Sen S, Keough K, Gibson J. Clinical reasoning: novel GLUT1-DS mutation refractory seizures and ataxia. Am Acad Neurol. 2015;84:e111–e114.
  • Raja M, Kinne RK. Pathogenic mutations causing glucose transport defects in GLUT1 transporter: the role of intermolecular forces in protein structure-function. Biophys Chem. 2015;200–201:9–17.
  • Yang H, Wang D, Engelstad K, et al. Glut1 deficiency syndrome and erythrocyte glucose uptake assay. Ann Neurol. 2011;70:996–1005.
  • Rohr K. Familial panmyelophthisis, Fanconi syndrome in adults. Blood. 1949;4:130–141.
  • Santer R, Schneppenheim R, Dombrowske A, Gotzer H, Steinmann B, Schaub J. Mutation in GLUT2, the gene for the liver-type glucose transporter, in patients with Fanconi-Bickel syndrome. Nat Genet. 1997;15:57–61.
  • De los Angeles García M, Millán C, Balmaceda-Aguilera C, et al. Hypothalamic ependymal-glial cells express the glucose transporter GLUT2, a protein involved in glucose sensing. J Neurochem. 2003;86:709–724.
  • Ohtsubo K, Takamatsu S, Gao C, Korekane H, Kurosawa TM, Taniguchi N. N-glycosylation modulates the membrane sub-domain distribution and activity of glucose transporter 2 in pancreatic beta cells. Biochem Biophys Res Comm. 2013;434:346–351.
  • Abbasi F, Azizi F, Javaheri M, Mosallanejad A, Ebrahim-Habibi A, Ghafouri-Fard S. Segregation of a novel homozygous 6 nucleotide deletion in GLUT2 gene in a Fanconi–Bickel syndrome family. Gene. 2015;557:103–105.
  • Matsuo H, Chiba T, Nagamori S, et al. Mutations in glucose transporter 9 gene SLC2A9 cause renal hypouricemia. Am J Hum Genet. 2008;83:744–751.
  • Jeannin G, Chiarelli N, Gaggiotti M, et al. Recurrent exercise-induced acute renal failure in a young Pakistani man with severe renal hypouricemia and SLC2A9 compound heterozygosity. BMC Med Genet. 2014:15:1–8.
  • Mou L, Jiang L, Hu Y. A novel homozygous GLUT9 mutation cause recurrent exercise-induced acute renal failure and posterior reversible encephalopathy syndrome. J Nephrol. 2015;28:387–392.
  • Stiburkova B, Ichida K, Sebesta I. Novel homozygous insertion in SLC2A9 gene caused renal hypouricemia. Mol Genet Metab. 2011;102:430–435.
  • Dinour D, Gray NK, Ganon L, et al. Two novel homozygous SLC2A9 mutations cause renal hypouricemia type 2. Nephrol Dial Transplant. 2012;27:1035–1041.
  • Stiburkova B, Taylor J, Marinaki AM, Sebesta I. Acute kidney injury in two children caused by renal hypouricaemia type 2. Pediatr Nephrol. 2012;27:1411–1415.
  • Dinour D, Gray NK, Campbell S, et al. Homozygous SLC2A9 mutations cause severe renal hypouricemia. J Am Soc Nephrol. 2010;21:64–72.
  • Warburg O. On the origin of cancer cells. Oncologia. 1956;9:75–83.
  • Racker E, Spector M. Warburg effect revisited: merger of biochemistry and molecular biology. Science. 1981;213:303–307.
  • Wang H, Li D, Liu S, et al. Small animal PET imaging of pancreatic cancer xenografts using 64Cu labeled monoclonal antibody MAb159. J Nucl Med. 2015:56:908–913.
  • Kepka L, Socha J. PET-CT use and the occurrence of elective nodal failure in involved field radiotherapy for non-small cell lung cancer: a systematic review. Radiother Oncol. 2015;115:151–156.
  • Koo HR, Park JS, Kang KW, Han W, Park IA, Moon WK. Correlation between 18F-FDG uptake on PET/CT and prognostic factors in triple-negative breast cancer. Eur Radiol. April 23, 2015. [Epub ahead of print.]
  • Weber WA, Gatsonis CA, Mozley PD, et al. Repeatability of 18F-FDG PET/CT in advanced non-small cell lung cancer: prospective assessment in two multicenter trials. J Nucl Med. April 23, 2015. [Epub ahead of print.]
  • Levi J, Cheng Z, Gheysens O, et al. Fluorescent fructose derivatives for imaging breast cancer cells. Bioconjug Chem. 2007;18:628–634.
  • Zamora-León SP, Golde D, Concha I, et al. Expression of the fructose transporter GLUT5 in human breast cancer. Proc Natl Acad Sci U S A. 1996;93:1847–1852.
  • Wuest M, Trayner BJ, Grant TN, et al. Radiopharmacological evaluation of 6-deoxy-6-[18F]fluoro-d-fructose as a radiotracer for PET imaging of GLUT5 in breast cancer. Nucl Med Biol. 2011;38:461–475.
  • Trayner BJ, Grant TN, West FG, Cheeseman CI. Synthesis and characterization of 6-deoxy-6-fluoro-d-fructose as a potential compound for imaging breast cancer with PET. Bioorg Med Chem. 2009;17:5488–5495.
  • Neves FA, Cortez E, Bernardo AF, et al. Heart energy metabolism impairment in Western-diet induced obese mice. J Nutr Biochem. 2014;25:50–57.
  • Aerni-Flessner L, Abi-Jaoude M, Koenig A, Payne M, Hruz PW. GLUT4, GLUT1, and GLUT8 are the dominant GLUT transcripts expressed in the murine left ventricle. Cardiovasc Diabetol. 2012;11:63–73.
  • Pereira RO, Wende AR, Olsen C, et al. Inducible overexpression of GLUT1 prevents mitochondrial dysfunction and attenuates structural remodeling in pressure overload but does not prevent left ventricular dysfunction. J Am Heart Assoc. 2013;2:e000301.
  • Craveiro M, Clerc I, Sitbon M, Taylor N. Metabolic pathways as regulators of HIV infection. Curr Opin HIV AIDS. 2013;8:182–189.
  • Loisel-Meyer S, Swainson L, Craveiro M, et al. Glut1-mediated glucose transport regulates HIV infection. Proc Natl Acad Sci U S A. 2012;109:2549–2554.
  • Palmer CS, Anzinger JJ, Zhou J, et al. Glucose transporter 1 expressing proinflammatory monocytes are elevated in combination antiretroviral therapy treated and untreated HIV+ subjects. J Immunol. 2014;193:5595–5603.
  • McBrayer SK, Cheng JC, Singhal S, Krett NL, Rosen ST, Shanmugam M. Multiple myeloma exhibits novel dependence on GLUT4, GLUT8, and GLUT11: implications for glucose transporter- directed therapy. Blood. 2012;119:4686–4697.
  • Aravinthan A, Challis B, Shannon N, Hoare M, Heaney J, Alexander GJ. Selective insulin resistance in hepatocyte senescence. Exp Cell Res. 2015;331:38–45.
  • Garvey WT, Maianu L, Zhu JH, Brechtel-Hook G, Wallace P, Baron AD. Evidence for defects in the trafficking and translocation of GLUT4 glucose transporters in skeletal muscle as a cause of human insulin resistance. J Clin Invest. 1998;101:2377–2386.
  • Favaretto F, Milan G, Collin GB, et al. GLUT4 defects in adipose tissue are early signs of metabolic alterations in alms1GT/GT, a mouse model for obesity and insulin resistance. PLoS One. 2014;9:e109540.