Molecular dynamics simulations of the human glucose transporter GLUT1

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Park, Min Sun ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 1; SUGAR; GLUCOSE; PROTEIN BINDING; SLC2A1 PROTEIN, HUMAN; WATER;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PROTEIN DOMAIN; SUGAR TRANSPORT; BINDING SITE; CHEMISTRY; ENZYME SPECIFICITY; HUMAN; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STRUCTURAL HOMOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

BINDING SITES; BIOLOGICAL TRANSPORT; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; WATER;

EID: 84928781442     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125361     Document Type: Article

References (69)

1. Reddy VS, Shlykov MA, Castillo R, Sun EI, Saier MH Jr. The major facilitator superfamily (MFS) revisited. Febs J. 2012; 279:2022-35. doi: 10.1111/j.1742-4658.2012.08588.x PMID: 22458847
2. Yan N. Structural advances for the major facilitator superfamily (MFS) transporters. Trends Biochem Sci. 2013; 38:151-9. doi: 10.1016/j.tibs.2013.01.003 PMID: 23403214
3. Augustin R. The protein family of glucose transport facilitators: It's not only about glucose after all. IUBMB life. 2010; 62:315-33. doi: 10.1002/iub.315 PMID: 20209635
4. Thorens B, Mueckler M. Glucose transporters in the 21st Century. Am J Physiol Endocrinol Metab. 2010; 298:E141-5. doi: 10.1152/ajpendo.00712.2009 PMID: 20009031
5. Birnbaum MJ, Haspel HC, Rosen OM. Cloning and characterization of a cDNA encoding the rat brain glucose-transporter protein. Proc Natl Acad Sci U S A. 1986; 83:5784-8. PMID: 3016720
6. Seidner G, Alvarez MG, Yeh JI, O'Driscoll KR, Klepper J, Stump TS, et al. GLUT-1 deficiency syndrome caused by haploinsufficiency of the blood-brain barrier hexose carrier. Nat Genet. 1998; 18:188-91. PMID: 9462754
7. Klepper J, Willemsen M, Verrips A, Guertsen E, Herrmann R, Kutzick C, et al. Autosomal dominant transmission of GLUT1 deficiency. Hum Mol Genet. 2001; 10:63-8. PMID: 11136715
8. Klepper J, Voit T. Facilitated glucose transporter protein type 1 (GLUT1) deficiency syndrome: impaired glucose transport into brain - a review. Eur J Pediatr. 2002; 161:295-304. PMID: 12029447
9. Overweg-Plandsoen WC, Groener JE, Wang D, Onkenhout W, Brouwer OF, Bakker HD, et al. GLUT-1 deficiency without epilepsy - an exceptional case. J Inherit Metab Dis. 2003; 26:559-63. PMID: 14605501
10. Klepper J, Wang D, Fischbarg J, Vera JC, Jarjour IT, O'Driscoll KR, et al. Defective glucose transport across brain tissue barriers: a newly recognized neurological syndrome. Neurochem Res. 1999; 24:587-94. PMID: 10227690
11. Klepper J, Monden I, Guertsen E, Voit T, Willemsen M, Keller K. Functional consequences of the autosomal dominant G272A mutation in the human GLUT1 gene. FEBS Lett. 2001; 498:104-9. PMID: 11389907
12. Brockmann K, Wang D, Korenke CG, von Moers A, Ho YY, Pascual JM, et al. Autosomal dominant glut-1 deficiency syndrome and familial epilepsy. Ann Neurol. 2001; 50:476-85. PMID: 11603379
13. Pascual JM, Van Heertum RL, Wang D, Engelstad K, De Vivo DC. Imaging the metabolic footprint of Glut1 deficiency on the brain. Ann Neurol. 2002; 52:458-64. PMID: 12325075
14. Wang D, Kranz-Eble P, De Vivo DC. Mutational analysis of GLUT1 (SLC2A1) in Glut-1 deficiency syndrome. Hum Mutat. 2000; 16:224-31. PMID: 10980529
15. Wang D, Yang H, Shi L, Ma L, Fujii T, Engelstad K, et al. Functional studies of the T295M mutation causing Glut1 deficiency: glucose efflux preferentially affected by T295M. Pediatr Res. 2008; 64:538-43. doi: 10.1203/PDR.0b013e318184d2b5 PMID: 18614966
16. Liu YY, Bao XH, Wang S, Fu N, Liu XY, Song FY, et al. [Clinical and genetic characteristics of glucose transporter type 1 deficiency syndrome]. Zhonghua Er Ke Za Zhi. 2013; 51:443-7. PMID: 24120063
17. Schwartzenberg-Bar-Yoseph F, Armoni M, Karnieli E. The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression. Cancer Res. 2004; 64:2627-33. PMID: 15059920
18. Deng D, Xu C, Sun P, Wu J, Yan C, Hu M, et al. Crystal structure of the human glucose transporter GLUT1. Nature. 2014; 510:121-5. doi: 10.1038/nature13306 PMID: 24847886
19. Maiden MC, Davis EO, Baldwin SA, Moore DC, Henderson PJ. Mammalian and bacterial sugar transport proteins are homologous. Nature. 1987; 325:641-3. PMID: 3543693
20. Lam VM, Daruwalla KR, Henderson PJ, Jones-Mortimer MC. Proton-linked D-xylose transport in Escherichia coli. J Bacteriol. 1980; 143:396-402. PMID: 6995439
21. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S. Structure and mechanism of the lactose permease of Escherichia coli. Science. 2003; 301:610-5. PMID: 12893935
22. Huang Y, Lemieux MJ, Song J, Auer M, Wang DN. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science. 2003; 301:616-20. PMID: 12893936
23. Sun L, Zeng X, Yan C, Sun X, Gong X, Rao Y, et al. Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature. 2012; 490:361-6. doi: 10.1038/nature11524 PMID: 23075985
24. Quistgaard EM, Low C, Moberg P, Tresaugues L, Nordlund P. Structural basis for substrate transport in the GLUT-homology family of monosaccharide transporters. Nat Struct Mol Biol. 2013; 20:766-8. doi: 10.1038/nsmb.2569 PMID: 23624861
25. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol. 1993; 234:779-815. PMID: 8254673
26. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A. Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct. 2000; 29:291-325. PMID: 10940251
27. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22:4673-80. PMID: 7984417
28. Muraoka A, Hashiramoto M, Clark AE, Edwards LC, Sakura H, Kadowaki T, et al. Analysis of the structural features of the C-terminus of GLUT1 that are required for transport catalytic activity. Biochem J. 1995; 311 (Pt 2):699-704.
29. Lovell SC, Davis IW, Arendall WB 3rd, de Bakker PI, Word JM, Prisant MG, et al. Structure validation by Calpha geometry: phi,psi and Cbeta deviation. Proteins. 2003; 50:437-50. PMID: 12557186
30. Gordon JC, Myers JB, Folta T, Shoja V, Heath LS, Onufriev A. H++: a server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Res. 2005; 33:W368-71. PMID: 15980491
31. Wille-Jorgensen P, Kjaergaard J, Thorup J, Jorgensen T, Fogh J, Munck O, et al. Heparin with and without dihydroergotamine in prevention of thromboembolic complications of major abdominal surgery. A randomized trial. Arch Surg. 1983; 118:926-8. PMID: 6347123
32. Jojart B, Martinek TA. Performance of the general amber force field in modeling aqueous POPC membrane bilayers. J Comput Chem. 2007; 28:2051-8. PMID: 17431937
33. Pantano S, Carafoli E. The role of phosphorylation on the structure and dynamics of phospholamban: a model from molecular simulations. Proteins. 2007; 66:930-40. PMID: 17154419
34. Cieplak P, Cornell WD, Bayly C, Kollman PA. Application of the Multimolecule and Multiconformational Resp Methodology to Biopolymers - Charge Derivation for DNA, Rna, and Proteins. J Comput Chem. 1995; 16:1357-77.
35. Hoover WG. Canonical dynamics: Equilibrium phase-space distributions. Phys Rev A. 1985; 31:1695-7. PMID: 9895674
36. Ponder JW, Case DA. Force fields for protein simulations. Adv Protein Chem. 2003; 66:27-85. PMID: 14631816
37. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. A Smooth Particle Mesh Ewald Method. J Chem Phys. 1995; 103:8577-93.
38. Pierce LC, Salomon-Ferrer R, Augusto FdOC, McCammon JA, Walker RC. Routine Access to Millisecond Time Scale Events with Accelerated Molecular Dynamics. J Chem Theory Comput. 2012; 8:2997-3002. PMID: 22984356
39. Tikhonova IG, Selvam B, Ivetac A, Wereszczynski J, McCammon JA. Simulations of Biased Agonists in the beta2 Adrenergic Receptor with Accelerated Molecular Dynamics. Biochemistry. 2013; 52:5593-603. doi: 10.1021/bi400499n PMID: 23879802
40. Roux B, Schulten K. Computational studies of membrane channels. Structure. 2004; 12:1343-51. PMID: 15296727
41. Lee HS, Robinson RC, Joo CH, Lee H, Kim YK, Choe H. Targeted molecular dynamics simulation studies of calcium binding and conformational change in the C-terminal half of gelsolin. Biochemical and biophysical research communications. 2006; 342:702-9. PMID: 16494841
42. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, et al. Scalable molecular dynamics with NAMD. J Comput Chem. 2005; 26:1781-802. PMID: 16222654
43. Hoover WG. Canonical dynamics: Equilibrium phase-space distributions. Phys Rev A. 1985; 31:1695-7. PMID: 9895674
44. Jarzynski C. Nonequilibrium equality for free energy differences. Phys Rev Lett. 1997; 78:2690-3.
45. Jarzynski C. Equilibrium free-energy differences from nonequilibrium measurements: A master-equation approach. Phys Rev E. 1997; 56:5018-35.
46. Ytreberg FM, Zuckerman DM. Efficient use of nonequilibrium measurement to estimate free energy differences for molecular systems. J Comput Chem. 2004; 25:1749-59. PMID: 15362132
47. Srinivasan J, Cheatham TE, Cieplak P, Kollman PA, Case DA. Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices. J Am Chem Soc. 1998; 120:9401-9.
48. Kollman PA, Massova I, Reyes C, Kuhn B, Huo S, Chong L, et al. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Accounts of chemical research. 2000; 33:889-97. PMID: 11123888
49. Zoete V, Meuwly M, Karplus M. Study of the insulin dimerization: binding free energy calculations and per-residue free energy decomposition. Proteins. 2005; 61:79-93. PMID: 16080143
50. Schurmann 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; 36:12897-902. PMID: 9335548
51. Schneider SA, Paisan-Ruiz C, Garcia-Gorostiaga I, Quinn NP, Weber YG, Lerche H, et al. GLUT1 gene mutations cause sporadic paroxysmal exercise-induced dyskinesias. Movement disorders: official journal of the Movement Disorder Society. 2009; 24:1684-8. doi: 10.1002/mds.22507 PMID: 19630075
52. Pascual JM, Van Heertum RL, Wang D, Engelstad K, De Vivo DC. Imaging the metabolic footprint of Glut1 deficiency on the brain. Annals of neurology. 2002; 52:458-64. PMID: 12325075
53. Leen WG, Klepper J, Verbeek MM, Leferink M, Hofste T, van Engelen BG, et al. Glucose transporter-1 deficiency syndrome: the expanding clinical and genetic spectrum of a treatable disorder. Brain: a journal of neurology. 2010; 133:655-70. doi: 10.1093/brain/awp336 PMID: 20129935
54. Liu YY, Bao XH, Wang S, Fu N, Liu XY, Song FY, et al. [Clinical and genetic characteristics of glucose transporter type 1 deficiency syndrome]. Zhonghua er ke za zhi Chinese journal of pediatrics. 2013; 51:443-7. PMID: 24120063
55. 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; 274:10923-6. PMID: 10196171
56. Hruz PW, Mueckler MM. Cysteine-scanning mutagenesis of transmembrane segment 7 of the GLUT1 glucose transporter. J Biol Chem. 1999; 274:36176-80. PMID: 10593902
57. Hruz PW, Mueckler MM. Cysteine-scanning mutagenesis of transmembrane segment 11 of the GLUT1 facilitative glucose transporter. Biochemistry. 2000; 39:9367-72. PMID: 10924131
58. 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; 277:3498-503. PMID: 11713254
59. Doege H, Schurmann 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):289-93.
60. Mori H, Hashiramoto M, Clark AE, Yang J, Muraoka A, Tamori Y, et al. Substitution of tyrosine 293 of GLUT1 locks the transporter into an outward facing conformation. J Biol Chem. 1994; 269:11578-83. PMID: 8157690
61. Olsowski A, Monden I, Krause G, Keller K. Cysteine scanning mutagenesis of helices 2 and 7 in GLUT1 identifies an exofacial cleft in both transmembrane segments. Biochemistry. 2000; 39:2469-74. PMID: 10704196
62. Asano T, Katagiri H, Takata K, Lin JL, Ishihara H, Inukai K, et al. The role of N-glycosylation of GLUT1 for glucose transport activity. The Journal of biological chemistry. 1991; 266:24632-6. PMID: 1761560
63. Mueckler M, Weng W, Kruse M. Glutamine 161 of Glut1 glucose transporter is critical for transport activity and exofacial ligand binding. The Journal of biological chemistry. 1994; 269:20533-8. PMID: 8051152
64. Inukai K, Asano T, Katagiri H, Anai M, Funaki M, Ishihara H, et al. Replacement of both tryptophan residues at 388 and 412 completely abolished cytochalasin B photolabelling of the GLUT1 glucose transporter. The Biochemical journal. 1994; 302 (Pt 2):355-61. PMID: 8092986
65. Mueckler M, Makepeace C. Analysis of transmembrane segment 10 of the Glut1 glucose transporter by cysteine-scanning mutagenesis and substituted cysteine accessibility. The Journal of biological chemistry. 2002; 277:3498-503. PMID: 11713254
66. Hashiramoto M, Kadowaki T, Clark AE, Muraoka A, Momomura K, Sakura H, et al. Site-directed mutagenesis of GLUT1 in helix 7 residue 282 results in perturbation of exofacial ligand binding. The Journal of biological chemistry. 1992; 267:17502-7. PMID: 1517202
67. Loike JD, Cao L, Kuang K, Vera JC, Silverstein SC, Fischbarg J. Role of facilitative glucose transporters in diffusional water permeability through J774 cells. J Gen Physiol. 1993; 102:897-906. PMID: 8301262
68. Mueckler M, Makepeace C. Transmembrane segment 5 of the Glut1 glucose transporter is an amphipathic helix that forms part of the sugar permeation pathway. The Journal of biological chemistry. 1999; 274:10923-6. PMID: 10196171
69. 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; 280:39562-8. PMID: 16172126