Salt-bridge Dynamics Control Substrate-induced Conformational Change in the Membrane Transporter GlpT

Journal of Molecular Biology

Volumn 378, Issue 4, 2008, Pages 828-839

  Law, Christopher J ^a   Almqvist, Jonas ^b   Bernstein, Adam ^a   Goetz, Regina M ^a   Huang, Yafei ^c   Soudant, Celine ^a   Laaksonen, Aatto ^b   Hovmöller, Sven ^b   Wang, Da Neng ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

antiporter; major facilitator superfamily; membrane transport; molecular dynamics simulations; secondary active transport

Indexed keywords

CARRIER PROTEIN; GLYCEROPHOSPHATE TRANSPORTER; HISTIDINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; BINDING SITE; ENZYME SPECIFICITY; ESCHERICHIA COLI; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTON TRANSPORT;

EID: 41949130566     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.03.029     Document Type: Article

References (63)

1. Hayashi S., Koch J.P., and Lin E.C.C. Active transport of L-α-glycerophosphate in Escherichia coli. J. Biol. Chem. 239 (1964) 3098-3105
2. Lin E.C.C. Glycerol dissimilation and its regulation in bacteria. Ann. Rev. Microbiol. 30 (1976) 535-578
3. Rao N.N., Roberts M.F., Torriani A., and Yashphe J. Effect of glpT and glpD mutations on expression of the phoA gene in Escherichia coli. J. Bacteriol. 175 (1993) 74-79
4. Andersson S.G., Zomorodipour A., Andersson J.O., Sicheritz-Ponten T., Alsmark U.C., Podowski R.M., et al. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396 (1998) 133-140
5. Nilsson R.P., Beijer L., and Rutberg B. The glpT and glpQ genes of the glycerol regulon in Bacillus subtilis. Microbiology 140 (1994) 723-730
6. Song X.M., Forsgren A., and Janson H. Glycerol-3-phosphate transport in Haemophilus influenzae: cloning, sequencing, and transcription analysis of the glpT gene. Gene 215 (1998) 381-388
7. Venkatesan M.M., Alexander W.A., and Fernandez-Prada C. A Shigella flexneri invasion plasmid gene, ipgH, with homology to IS629 and sequences encoding bacterial sugar phosphate transport proteins. Gene 175 (1996) 23-27
8. Bevan M., Bancroft I., Bent E., Goodman H., Dean C., Bergkamp R., et al. Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391 (1998) 485-488
9. Bartoloni L., Wattenhofer M., Kudoh J., Berry A., Shibuya K., Kawasaki K., et al. Cloning and characterization of a putative human glycerol 3-phosphate permease gene (SLC37A1 or G3PP) on 21q22.3: Mutation analysis in two candidate phenotypes. DFNB10 and a glycerol kinase deficiency. Genomics 70 (2000) 190-200
10. Pao S.S., Paulsen I.T., and Saier M.H. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62 (1998) 1-34
11. Maloney P.C., Ambudkar S.V., Anatharam V., Sonna L.A., and Varadhachary A. Anion-exchange mechanisms in bacteria. Microbiol. Rev. 54 (1990) 1-17
12. Sa-Correia I., and Tenreiro S. The multidrug resistance transporters of the major facilitator superfamily, 6 years after disclosure of Saccharomyces cerevisiae genome sequence. J. Biotechnol. 98 (2002) 215-226
13. Saier Jr. M.H., Beatty J.T., Goffeau A., Harley K.T., Heijne W.H., Huang S.C., Jack D.L., et al. The major facilitator superfamily. J. Mol. Microbiol. Biotech. 1 (1999) 257-279
14. Abramson J., Smirnova I., Kasho V., Verner G., Kaback H.R., and Iwata S. Structure and mechanism of the lactose permease of Escherichia coli. Science 301 (2003) 610-615
15. Kaback H.R. A molecular mechanism for energy coupling in a membrane transport protein, the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 94 (1997) 5539-5543
16. Vidavar G.A. Inhibition of parallel flux and augmentation of counter flux shown by transport models not involving a mobile carrier. J. Theor. Biol. 10 (1966) 301-306
17. Lemieux M.J., Huang Y., and Wang D.N. Structural basis of substrate translocation by the Escherichia coli glycerol-3-phosphate transporter: a member of the major facilitator superfamily. Curr. Opin. Struct. Biol. 14 (2004) 405-412
18. Huang Y., Lemieux M.J., Song J., Auer M., and Wang D.N. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301 (2003) 616-620
19. Law C.J., Yang Q., Soudant C., Maloney P.C., and Wang D.N. Kinetic evidence is consistent with the rocker-switch mechanism of membrane transport by GlpT. Biochemistry 46 (2007) 12190-12197
20. Krupka R.M. Role of substrate binding forces in exchange-only transport systems: I. Transition-state theory. J. Membr. Biol. 109 (1989) 151-158
21. Krupka R.M. Role of substrate binding forces in exchange-only transport systems: II. Implications for the mechanism of the anion exchanger of red cells. J. Membr. Biol. 109 (1989) 159-171
22. Fann M.C., Davies A.H., Varadhachary A., Kuroda T., Sevier C., Tsuchiya T., and Maloney P.C. Identification of two essential arginine residues in UhpT, the sugar phosphate antiporter of Escherichia coli. J. Membr. Biol. 164 (1998) 187-195
23. Almqvist J., Huang Y., Hovmöller S., and Wang D.N. Homology modeling of the human microsomal glucose-6-phosphate transporter explains the mutations that cause the glycogen storage disease type Ib. Biochemistry 43 (2004) 9289-9297
24. Chen L.Y., Pan C.J., Shieh J.J., and Chou J.Y. Structure-function analysis of the glucose-6-phosphate transporter deficient in glycogen storage disease type Ib. Hum. Mol. Genet. 11 (2002) 3199-3207
25. Hall J.A., Fann M.C., and Maloney P.C. Altered substrate selectivity in a mutant of an intrahelical salt bridge in UhpT, the sugar phosphate carrier of Escherichia coli. J. Biol. Chem. 274 (1999) 6148-6153
26. i-linked sugar phosphate carrier of Escherichia coli. J. Biol. Chem. 280 (2005) 3376-3381
27. Auer M., Kim M.J., Lemieux M.J., Villa A., Song J., Li X.D., and Wang D.N. High-yield expression and functional analysis of Escherichia coli glycerol-3-phosphate transporter. Biochemistry 40 (2001) 6628-6635
28. Fann M.C., Busch A., and Maloney P.C. Functional characterization of cysteine residues in GlpT, the glycerol 3-phosphate transporter of Escherichia coli. J. Bacteriol. 185 (2003) 3863-3870
29. Riordan J.F. Arginyl residues and anion binding sites in proteins. Mol. Cell. Biochem. 26 (1979) 71-92
30. Skarzynski T., Mistry A., Wonacott A., Hutchinson S.E., Kelly V.A., and Duncan K. Structure of UDP-N-acetylglucosamine enolpyruvyl transferase, an enzyme essential for the synthesis of bacterial peptidoglycan, complexed with substrate UDP-N-acetylglucosamine and the drug fosfomycin. Structure 4 (1996) 1465-1474
31. Wang X., Sarker R.I., and Maloney P.C. Analysis of substrate-binding elements in OxlT, the oxalate:formate antiporter of Oxalobacter formigenes. Biochemistry 45 (2006) 10344-10350
32. Unkles S.E., Rouch D.A., Wang Y., Siddiqi M.Y., Glass A.D., and Kinghorn J.R. Two perfectly conserved arginine residues are required for substrate binding in a high-affinity nitrate transporter. Proc. Natl. Acad. Sci. USA 101 (2004) 17549-17554
33. Jia W., and Cole J.A. Nitrate and nitrite transport in Escherichia coli. Biochem. Soc. Trans. 33 (2005) 159-161
34. Van Winkle L.J. Transport kinetics. Biomembrane Transport (1995), Academic Press, New York 90-91
35. Schneider F. Histidine in enzyme active centers. Angew. Chem. Int. Ed. Engl. 17 (1978) 583-592
36. Padan E., Sarkar H.K., Viitanen P.V., Poonian M.S., and Kaback H.R. Site-specific mutagenesis of histidine residues in the lac permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 82 (1985) 6765-6768
37. + antiporter. Biochemistry 35 (1996) 4359-4364
38. Shirvan A., Laskar O., Steiner-Mordoch S., and Schuldiner S. Histidine-419 plays a role in energy coupling in the vesicular monoamine transporter from rat. FEBS Lett. 356 (1994) 145-150
39. Dietz K.J., Canut H., and Marigo G. Identification of an essential histidine residue at the active site of the tonoplast malate carrier in Catharanthus roseus cells. J. Membr. Biol. 129 (1992) 137-143
40. + exchanger of fission yeast. Biochemistry 37 (1998) 8282-8288
41. + antiporter in Escherichia coli. Proc. Natl. Acad. Sci. USA 90 (1993) 1212-1216
42. Poolman B., Modderman R., and Reizer J. Lactose transport system of Streptococcus thermophilus. The role of histidine residues. J. Biol. Chem. 267 (1992) 9150-9157
43. Pourcher T., Sarkar H.K., Bassilana M., Kaback H.R., and Leblanc G. Histidine-94 is the only important histidine residue in the melibiose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 87 (1990) 468-472
44. Coster H.G., and Chilcott T.C. Electric field effects in proteins in membranes. Bioelectrochemistry 56 (2002) 141-146
45. Cymes G.D., Ni Y., and Grosman C. Probing ion-channel pores one proton at a time. Nature 438 (2005) 975-980
46. Dougherty D.A. Cation-π interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271 (1996) 163-168
47. Loewenthal R., Sancho J., and Fersht A.R. Histidine-aromatic interactions in barnase. Elevation of histidine pKa and contribution to protein stability. J. Mol. Biol. 224 (1992) 759-770
48. 1H NMR spectroscopy and computer simulations To analyze histidine pKa changes in a protein tyrosine phosphatase: experimental and theoretical determination of electrostatic properties in a small protein. Biochemistry 36 (1997) 11984-11994
49. +-peptide transporter PepT1. Biochem. Biophys. Res. Comm. 272 (2000) 726-730
50. Fann M.C., and Maloney P.C. The functional symmetry of UhpT, the sugar phosphate transporter of Escherichia coli. J. Biol. Chem. 273 (1998) 33735-33740
51. + symport in LacY. EMBO J. 25 (2006) 1177-1183
52. Tieleman D.P., Forrest L.R., Sansom M.S., and Berendsen H.J. Lipid properties and the orientation of aromatic residues in OmpF, influenza M2, and alamethicin systems: molecular dynamics simulations. Biochemistry 37 (1998) 17554-17561
53. Morris G.M., Goodsell D.S., Halliday R.S., Huey R., Hart W.E., Belew R.K., and Olson A.J. Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J. Comp. Chem. 19 (1998) 1639-1662
54. Schuttelkopf A.W., and Van Aalten D.M. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta. Cryst. D 60 (2004) 1355-1363
55. Dupradeau F.Y., Cezard C., Lelong R., Stanislawiak E., Pecher J., Delepine J.C., and Cieplak P. R.E.DD.B.: A database for RESP and ESP atomic charges, and force field libraries. Nucleic Acids Res. 36 (2008) D360-D367
56. Berendsen H.J.C., Van der Spoel D., and Van Drunen R. Gromacs - a message-passing parallel molecular dynamics implementation. Comp. Phys. Comm. 91 (1995) 43-56
57. Lindahl E., Hess B., and Van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Mod. 7 (2001) 306-317
58. Berger O., Edholm O., and Jahnig F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72 (1997) 2002-2013
59. Berendsen H.J.C., Postma J.P.M., Van Gunsteren W.F., and Hermans J. Interaction models for water in relation to protein hydration. In: Pullman B. (Ed). Intermolecular Forces (1981), D. Reidel Publishing Company, Dordrecht 331-342
60. Essman U., Perera L., Berkowitz M., Darden T., Lee H., and Pedersen L. A smooth particle mesh Ewald method. J. Chem. Phys. 103 (1995) 8577-8593
61. Hess B., Bekker H., Berendsen H.J.C., and Fraaije J.G.E.M. LINCS: A linear constraint solver for molecular simulations. J. Comp. Chem. 18 (1997) 1463-1472
62. Miyamoto S., and Kollman P.A. Settle - an analytical version of the shake and rattle algorithm for rigid water models. J. Comp. Chem. 13 (1992) 952-962
63. Berendsen H.J.C., Postma J.P.M., Van Gunsteren W.F., DiNola A., and Haak J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81 (1984) 3684-3690