Three-dimensional crystallization of the Escherichia coli glycerol-3-phosphate transporter: A member of the major facilitator superfamily

Protein Science

Volumn 12, Issue 12, 2003, Pages 2748-2756

  Lemieux, M Joanne ^a,b   Song, Jinmei ^a   Kim, Myong Jin ^a,c   Huang, Yafei ^a   Villa, Anthony ^a,d   Auer, Manfred ^a   Li, Xiao Dan ^a,e   Wang, Da Neng ^a  

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

^b UNIVERSITY OF ALBERTA   (Canada)

^c Principled Capital Management   (United States)

^d A Subsidiary of Lantheus Holdings   (United States)

^e PAUL SCHERRER INSTITUTE   (Switzerland)

Author keywords

Crystallization; Detergent; Lipid; Membrane protein; Transporter

Indexed keywords

CARDIOLIPIN; GLYCEROPHOSPHATE; MACROGOL; PHOSPHATE; PHOSPHATE TRANSPORTER; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL; PHOSPHOLIPID; PROTEIN;

ARTICLE; BACTERIAL MEMBRANE; CRYSTALLIZATION; ESCHERICHIA COLI; GEL PERMEATION CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FAMILY; X RAY CRYSTALLOGRAPHY;

CHROMATOGRAPHY, AFFINITY; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DETERGENTS; ESCHERICHIA COLI; MEMBRANE TRANSPORT PROTEINS; PHOSPHOLIPIDS; RECOMBINANT FUSION PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0345276579     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.03276603     Document Type: Article

References (48)

1. Ambudkar, S.V., Larson, T.J., and Maloney, P.C. 1986a. Reconstitution of sugar phosphate transport systems of Escherichia coli. J. Biol. Chem. 261: 9083-9086.
2. Ambudkar, S.V., Sonna, L.A., and Maloney, P.C. 1986b. Variable stoichiometry of phosphate-linked anion exchange in Streptococcus lactis: Implications for the mechanism of sugar phosphate transport by bacteria. Proc. Natl. Acad. Sci. 83: 280-284.
3. Auer, M., Kim, M.J., Lemieux, M.J., Villa, A., Song, J., Li, X.D., and Wang, D.N. 2001. High-yield expression and functional analysis of Escherichia coli glycerol-3-phosphate transporter. Biochemistry 40: 6628-6635.
4. Boulter, J.M. and Wang, D.N. 2001. Purification and characterization of human erythrocyte glucose transporter in decylmaltoside detergent solution. Protein Expr. Purif. 22: 337-348.
5. Cadene, M. and Chait, B. 2000. A robust, detergent friendly method for mass spectrometry analysis of integral membrane proteins. Anal. Chem. 72: 5655-5658.
6. Carter Jr., C.W. and Carter, C.W. 1979. Protein crystallization using incomplete factorial experiments. J. Biol. Chem. 254: 12219-12223.
7. Chang, G., Spencer, R.H., Lee, A.T., Barclay, M.T., and Rees, D.C. 1998. Structure of the MscL homolog from Mycobacterium tubeculosis: A gated mechanosensitive ion channel. Science 282: 2220-2226.
8. Chen, P.S., Toribara, T.Y., and Warner, H. 1956. Microdetermination of phosphorous. Anal. Chem. 28: 1756-1758.
9. Devaux, P.F. and Seigneuret, M. 1985. Specificity of lipid-protein interactions as determined by spectroscopic techniques. Biochim. Biophys. Acta 822: 63-125.
10. + conduction and selectivity. Science 280: 69-77.
11. Elvin, C.M., Hardy, C.M., and Rosenberg, H. 1985. π exchange mediated by the GlpT-dependent sn-glycerol-3-phosphate transport system in Escherichia coli. J. Bacteriol. 161: 1054-1058.
12. Engel, C.K., Chen, L., and Prive, G.G. 2002. Stability of the lactose permease in detergent solutions. Biochim. Biophys. Acta 1564: 47-56.
13. Folch, J., Lees, M., and Stanley, G.H.S. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497-509.
14. Garavito, R.M. and Rosenbusch, J.P. 1980. Three-dimensional crystals of an integral membrane protein: An initial x-ray analysis. J. Cell. Biol. 86: 327-329.
15. Garavito, R.M., Picot, D., and Loll, P.J. 1996. Strategies for crystallizing membrane proteins. J. Bioenerg. Biomemb. 28: 13-27.
16. Gött, P. and Boos, W. 1988. The transmembrane topology of the sn-glycerol-3-phosphate permease of Escherichia coli analysed by phoA and lacZ protein fusions. Mol. Microbiol. 2: 655-663.
17. Henderson, P.J.F. 1993. The 12-transmembrane helix transporters. Curr. Opin. Cell Biol. 5: 708-712.
18. Huang, Y., Lemieux, M.J., Song, J., Auer, M., and Wang, D.N. 2003. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301: 616-620.
19. Jancarik, J., Scott, W.G., Milligan, D.L., Koshland, D.E., and Kim, S.H. 1991. Crystallization and preliminary X-ray diffraction study of the ligand-binding domain of the bacterial chemotaxis-mediating aspartate receptor of Salmonella typhimurium. J. Mol. Biol. 221: 31-34.
20. Koronakis, V., Sharff, A., Koronakis, E., Luisi, B., and Hughes, C. 2000. Crystal structure of the bacterial membrane protein TolC central to multi-drug efflux and protein export. Nature 405: 914-919.
21. Kühlbrandt, W. 1987. Three-dimensional crystals of the light-harvesting chlorophyll a/b protein complex from pea chloroplasts. J. Mol. Biol. 194: 757-762.
22. -. 1988. The structure of light-harvesting chlorophyll a/b protein complex from plant photosynthetic membranes at 7Å resolution in projection. J. Mol. Biol. 202: 849-864.
23. Kwong, P.D., Wyatt, R., Desjardins, E., Robinson, J., Culp, J.S., Hellmig, B.D., Sweet, R.W., Sodroski, J., and Hendrickson, W.A. 1999. Probability analysis of variational crystallization and its application to gp120, the exterior envelope glycoprotein of type 1 human immunodeficiency virus (HIV-1). J. Biol. Chem. 274: 4115-4123.
24. Lancaster, C.R., Kroger, A., Auer, M., and Michel, H. 1999. Structure of fumarate reductase from Wolinella succinogenes at 2.2 Å resolution. Nature 402: 377-385.
25. Larson, T.J., Schumacher, G., and Boos, W. 1982. Identification of the glpT-encoded sn-glycerol-3-phosphate permease of Escherichia coli, an oligomeric integral membrane protein. J. Bacteriol. 152: 1008-1021.
26. Lemieux, M.J., Reithmeier, R.A., and Wang, D.N. 2002. Importance of detergent and phospholipid in the crystallization of the human erythrocyte anion-exchanger membrane domain. J. Struct. Biol. 137: 322-332.
27. Li, X.D., Villa, A., Gownley, C., Kim, M.J., Song, J.M., Auer, M., and Wang, D.N. 2001. Monomeric state and ligand binding of recombinant GABA transporter from Escherichia coli. FEBS Lett. 494: 165-169.
28. Locher, K.P., Lee, A.T., and Rees, D.C. 2002. The E. coli BtuCD structure: A framework for ABC transporter architecture and mechanism. Science 296: 1091-1098.
29. McPherson, A. 1990. Current approaches to macromolecular crystallization. Eur. J. Biochem. 189: 1-23.
30. -. 1999. Crystallization of biological macromolecules. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Michel, H. 1982. Three-dimensional crystals of a membrane protein complex. J. Mol. Biol. 158: 567-572.
32. -. 1983. Crystallization of membrane proteins. Trends Biochem. Sci. 8: 56-59.
33. Michel, H. and Oesterhelt, D. 1980. Three-dimensional crystals of membrane proteins: Bacteriorhodopsin. Proc. Natl. Acad. Sci. 77: 1283-1285.
34. Otwinowski, Z. and Miror, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Meth. Enzymol. 276: 307-326.
35. Pao, S.S., Paulsen, I.T., and Saier Jr., M.H. 1998. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62: 1-34.
36. Qiagen. 2001. QIAgen detection and assay handbook, pp. 35-37. Qiagen, Hilden, Germany.
37. Reiss-Husson, F. 1991. Crystallization of membrane proteins. In Crystallization of nucleic acids and proteins (eds. A. Ducruix and R. Geige), pp. 175-193. IRL Press, Oxford.
38. Reizer, J., Finley, K., Kakuda, D., MacLeod, C.L., Reizer, A., and Saier Jr., M.H. 1993. Mammalian integral membrane receptors are homologous to facilitators and antiporters of yeast, fungi, and eubacteria. Protein Sci. 2: 20-30.
39. Rock, C.O. and Cronan, J.E. 1985. Lipid metabolism in prokaryotes. In Biochemistry of lipids and membranes (eds. D.E. Vance and J.E. Vance), pp. 73-115. Benjamin/Cummings, Menlo Park, CA.
40. Rosenbusch, J.P., Lustig, A., Grabo, M., Zulauf, M., and Regenass, M. 2001. Approaches to determining membrane protein structures to high resolution: Do selections of subpopulations occur? Micron 32: 75-90.
41. Schertler, G.F.X., Bartunik, H.D., Michel, H., and Oesterhelt, D. 1993. Orthorhombic crystal form of bacteriorhodopsin nucleated on benzamidine diffracting to 3.6 Å resolution. J. Mol. Biol. 234: 156-164.
42. Silhavy, T.J., Hartig-Beecken, I., and Boos, W. 1976. Periplasmic protein related to the sn-glycerol-3-phosphate transport system of Escherichia coli. J. Bacteriol. 126: 951-958.
43. Song, L. and Gouaux, J.E. 1997. Membrane protein crystallization: Application of sparse matrices to the a-hemolysin heptamer. In Methods in enzymology (eds. C.W. Carter Jr. and R.M. Sweet), pp. 60-74. Academic Press, San Diego, CA.
44. + channel. Biochemistry 41: 10771-10777.
45. Wang, D.N., Lemieux, M.J., and Boulter, J.M. 2003a. Purification and characterization of transporter proteins from human erythrocyte membrane. In Membrane protein protocols: Expression, purification and characterization (ed. B. Selinsky), pp. 239-256. Humana Press, Totowa, NJ.
46. Wang, D.N., Safferling, M., Lemieux, M.J., Griffith, H., Chen, Y., and Li, X.D. 2003b. Practical aspects of overexpressing bacterial secondary membrane transporters for structural studies. Biochim. Biophys. Acta 1610: 23-36.
47. Wiener, M.C. and Snook, C.F. 2001. The development of membrane protein crystallization screens based on detergent solution properties. J. Cryst. Growth 232: 426-431.
48. Zulauf, M. 1991. Detergent phenomena in membrane protein crystallization. In Crystallization of membrane proteins (ed. H. Michel), pp. 53-72. CRC Press, Boca Raton, FL.