848
Views
10
CrossRef citations to date
0
Altmetric
Research Article

TROSY NMR with a 52 kDa sugar transport protein and the binding of a small-molecule inhibitor

, , , , &
Pages 131-140 | Received 12 Dec 2013, Accepted 05 Mar 2014, Published online: 07 May 2014

References

  • Appleyard AN, Herbert RB, Henderson PJ, Watts A, Spooner PJR. 2000. Selective NMR observation of inhibitor and sugar binding to the galactose-H+ symport protein GalP, of Escherichia coli. Biochim Biophys Acta 1509:55–64
  • Bahar I, Lezon TR, Bakan A, Shrivastava IH. 2010. Normal mode analysis of biomolecular structures: functional mechanisms of membrane proteins. Chem Rev 110:1463–1497
  • Bakheet TM, Doig AJ. 2009. Properties and identification of human protein drug targets. Bioinformatics 25:451–457
  • Baldwin SA, Henderson PJ. 1989. Homologies between sugar transporters from eukaryotes and prokaryotes. Annu Rev Physiol 51:459–471
  • Büttner M. 2007. The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Lett 581:2318–2324
  • Craven CJ, Al-Owais M, Parker MJ. 2007. A systematic analysis of backbone amide assignments achieved via combinatorial selective labelling of amino acids. J Biomol NMR 38:151–159
  • Dalvit C, Pevarello P, Tatò M, Veronesi M, Vulpetti A, Sundström M. 2000. Identification of compounds with binding affinity to proteins via magnetization transfer from bulk water. J Biomol NMR 18:65–68
  • Drews J. 2000. Drug discovery: a historical perspective. Science 287:1960–1964
  • Fagerberg L, Jonasson K, von Heijne G, Uhlen M, Berglund L. 2010. Prediction of the human membrane proteome. Proteomics 10:1141–1149
  • Fernández C, Hilty C, Wider G, Güntert P, Wüthrich K. 2004. NMR structure of the integral membrane protein OmpX. J Mol Biol 336:1211–1221
  • Gautier A, Kirkpatrick JP, Nietlispach D. 2008. Solution-state NMR spectroscopy of a seven-helix transmembrane protein receptor: backbone assignment, secondary structure, and dynamics. Angew Chem Int Ed 47:7297–7300
  • Gautier A, Mott HR, Bostock MJ, Kirkpatrick JP, Nietlispach D. 2010. Structure determination of the seven-helix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat Struct Mol Biol 17:768–775
  • Guo C, Zhang D, Tugarinov V. 2008. An NMR experiment for simultaneous TROSY-based detection of amide and methyl groups in large proteins. J Am Chem Soc 130:10872–10873
  • Hefke F, Bagaria A, Reckel S, Ullrich SJ, Dötsch V, Glaubitz C, Güntert P. 2011. Optimization of amino acid type-specific 13C and 15N labeling for the backbone assignment of membrane proteins by solution- and solid-state NMR with the UPLABEL algorithm. J Biomol NMR 49:75–84
  • Henderson PJ. 1990. Proton-linked sugar transport systems in bacteria. J Bioenerg Biomembr 22:525–569
  • Henderson PJ, Baldwin SA. 2012. Structural biology: bundles of insights into sugar transporters. Nature 490:348–350
  • Henderson PJ, Baldwin SA. 2013. This is about the in and the out. Nat Struct Mol Biol 20:654–655
  • Henderson PJ, Macpherson AJ. 1986. Assay, genetics, proteins and reconstitution of proton-linked galactose, arabinose and xylose transport systems of Escherichia coli. Methods Enzymol 125:387–429
  • Hopkins AL, Groom CR. 2002. The druggable genome. Nat Rev Drug Discov 1:727–730
  • Iancu CV, Zamoon J, Woo SB, Aleshin A, Choe JY. 2013. Crystal structure of a glucose/H+ symporter and its mechanism of action. Proc Natl Acad Sci USA 110:17862–17867
  • Kainosho M, Torizawa T, Iwashita Y, Terauchi T, Mei Ono A, Güntert P. 2006. Optimal isotope labelling for NMR protein structure determinations. Nature 440:52–57
  • Kang C, Li Q. 2011. Solution NMR study of integral membrane proteins. Curr Opin Chem Biol 15:560–569
  • Kay LE. 2011. Solution NMR spectroscopy of supra-molecular systems, why bother? A methyl-TROSY view. J Magn Reson 210:159–170
  • Kim H-.J, Howell SC, Van Horn, WD, Ho Jeon Y, Sanders CR. 2009. Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins. Prog Nucl Mag Res Sp 55:335–360
  • Klammt C, Maslennikov I, Bayrhuber M, Eichmann C, Vajpai N, Chiu EJ, et al. 2012. Facile backbone structure determination of human membrane proteins by NMR spectroscopy. Nat Methods 9:834–839
  • Konrat R, Yang D, Kay LE. 1999. A 4D TROSY-based pulse scheme for correlating 1HNi, 15Ni, 13Cαi, 13C′i−1 chemical shifts in high molecular weight, 15N, 13C, 2H labeled proteins. J Biomol NMR 15:309–313
  • Korzhnev DM, Kloiber K, Kanelis V, Tugarinov V, Kay LE. 2004. Probing slow dynamics in high molecular weight proteins by methyl-TROSY NMR spectroscopy: application to a 723-residue enzyme. J Am Chem Soc 126:3964–3973
  • Kurze AK, Galliciotti G, Heine C, Mole SE, Quitsch A, Braulke T. 2010. Pathogenic mutations cause rapid degradation of lysosomal storage disease-related membrane protein CLN6. Human Mutat 31:E1163–E1174
  • Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
  • Li F, Ma C, Wang X, Gao C, Zhang J, Wang Y, et al. 2011. Characterization of Sucrose transporter alleles and their association with seed yield-related traits in Brassica napus L. BMC Plant Biol 11:168
  • Liu JF, Rost B. 2001. Comparing function and structure between entire proteomes. Prot Sci 10:1970–1979
  • Lundstrom K. 2006. Latest development in drug discovery on G protein-coupled receptors. Curr Protein Pept Sci 7:465–470
  • Macpherson AJ, Jones-Mortimer MC, Horne P, Henderson PJ. 1983. Identification of the GalP galactose transport protein of Escherichia coli. J Biol Chem 258:4390–4396
  • Maiden MC, Davis EO, Baldwin SA, Moore DC, Henderson PJ. 1987. Mammalian and bacterial sugar transport proteins are homologous. Nature 325:641–643
  • Martin GM, Seamon KB, Brown FM, Shanahan MF, Roberts PE, Henderson PJ. 1994. Forskolin specifically inhibits the bacterial galactose-H+ symport protein, GalP, of Escherichia coli. J Biol Chem 269:24870–24877
  • Martin GM, Walmsley AR, Henderson PJ. 1995. The kinetics and thermodynamics of the binding of forskolin to the galactose-H+ transport protein, GalP, of Escherichia coli. Biochem J 308:261–268
  • Maslennikov I, Klammt C, Hwang E, Kefala G, Okamura M, Esquivies L, et al. 2010. Membrane domain structures of three classes of histidine kinase receptors by cell-free expression and rapid NMR analysis. Proc Natl Acad Sci USA 107:10902–10907
  • Maslennikov I, Choe S. 2013. Advances in NMR structures of integral membrane proteins. Curr Opin Struct Biol 23:555–562
  • McDonald TP, Walmsley AR, Martin GE, Henderson PJ. 1995. The role of tryptophans 371 and 395 in the binding of antibiotics and the transport of sugars by the D-galactose-H+ symport protein (GalP) from Escherichia coli. J Biol Chem 270:30359–30370
  • Ng DP, Poulsen BE, Deber CM. 2012. Membrane protein misassembly in disease. Biochim Biophys Acta 1818:1115–1122
  • Nietlispach D, Gautier A. 2011. Solution NMR studies of polytopic α-helical membrane proteins. Curr Opin Struct Biol 21:497–508
  • Ollerenshaw JE, Tugarinov V, Skrynnikov NR, Kay LE. 2005. Comparison of 13CH3, 13CH2D, and 13CHD2 methyl labeling strategies in proteins. J Biomol NMR 33:25–41
  • Overington JP, Al-Lazikani B, Hopkins AL. 2006. Opinion – how many drug targets are there? Nat Rev Drug Discov 5:993–996
  • Oxenoid K, Chou JJ. 2013. The present and future of solution NMR in investigating the structure and dynamics of channels and transporters. Curr Opin Struct Biol 23:547–554
  • Ozcan S, Johnston M. 1999. Function and regulation of yeast hexose transporters. Microbiol Mol Biol Rev 63:554–569
  • Parker MJ, Aulton-Jones M, Hounslow AM, Craven CJ. 2004. A combinatorial selective labeling method for the assignment of backbone amide NMR resonances. J Am Chem Soc 602:275–292
  • Pascual JM, Wang D, Lecumberri B, Yang H, Mao X, Yang R, De Vivo DC. 2004. GLUT1 deficiency and other glucose transporter diseases. Eur J Endocrinol 150:627–633
  • Patching SG, Herbert RB, O’Reilly J, Brough AR, Henderson PJ. 2004. Low 13C-background for NMR-based studies of ligand binding using 13C-depleted glucose as carbon source for microbial growth: 13C-labeled glucose and 13C-forskolin binding to the galactose-H+ symport protein GalP in Escherichia coli. J Am Chem Soc 126:86–87
  • Patching SG, Henderson PJ, Herbert RB, Middleton DA. 2008a. Solid-state NMR spectroscopy detects interactions between tryptophan residues of the E. coli sugar transporter GalP and the alpha-anomer of the D-glucose substrate. J Am Chem Soc 130:1236–1244
  • Patching SG, Psakis G, Baldwin SA, Baldwin J, Henderson PJ, Middleton DA. 2008b. Relative substrate affinities of wild-type and mutant forms of the Escherichia coli sugar transporter GalP determined by solid-state NMR. Mol Membr Biol 25:474–484
  • Patching SG. 2011. NMR structures of polytopic integral membrane proteins. Mol Membr Biol 28:370–397
  • Patching SG, Henderson PJ, Sharples DJ, Middleton DA. 2013. Probing the contacts of a low-affinity substrate with a membrane-embedded transport protein using 1H-13C cross-polarisation magic-angle spinning solid-state NMR. Mol Membr Biol 30:129–137
  • Pervushin K, Riek R, Wider G, Wüthrich K. 1997. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci USA 94:12366–12371
  • Rask-Andersen M, Sällman Almén M, Schiöth HB. 2011. Trends in the exploitation of novel drug targets. Nat Rev Drug Discov 10:579–590
  • Reckel S, Sobhanifar S, Durst F, Löhr F, Shirokov VA, Dötsch V, Bernhard F. 2010. Strategies for the cell-free expression of membrane proteins. Methods Mol Biol 607:187–212
  • Reckel S, Gottstein D, Stehle J, Löhr F, Verhoefen MK, Takeda M, et al. 2011. Solution NMR structure of proteorhodopsin. Angew Chem Int Ed 50:11942–11946
  • Religa TL, Kay LE. 2010. Optimal methyl labeling for studies of supra-molecular systems. J Biomol NMR 47:163–169
  • Renault M, Saurel O, Czaplicki J, Demange P, Gervais V, Löhr F, et al. 2009. Solution state NMR structure and dynamics of KpOmpA, a 210 residue transmembrane domain possessing a high potential for immunological applications. J Mol Biol 385:117–130
  • Riek R, Wider G, Pervushin K, Wüthrich K. 1999. Polarization transfer by cross-correlated relaxation in solution NMR with very large molecules. Proc Natl Acad Sci USA 96:4918–4923
  • Riek R, Fiaux J, Bertelsen EB, Horwich AL, Wüthrich K. 2002. Solution NMR techniques for large molecular and supramolecular structures. J Am Chem Soc 124:12144–12153
  • Robichaud T, Appleyard AN, Herbert RB, Henderson PJ, Carruthers A. 2011. Determinants of ligand binding affinity and cooperativity at the GLUT1 endofacial site. Biochemistry 50:3137–3148
  • Rosenbaum DM, Rasmussen SF, Kobilka BK. 2009. The structure and function of G-protein-coupled receptors. Nature 459:356–363
  • Salzmann M, Pervushin K, Wider G, Senn H, Wüthrich K. 1998. TROSY in triple-resonance experiments: new perspectives for sequential NMR assignment of large proteins. Proc Natl Acad Sci USA 95:13585–13590
  • Salzmann M, Pervushin K, Wider G, Senn H, Wüthrich K. 1999a. [13C]-constant-time [15N, 1H]-TROSY-HNCA for sequential assignments of large proteins. J Biomol NMR 14:85–88
  • Salzmann M, Wider G, Pervushin K, Senn H, Wüthrich K. 1999b. TROSY-type triple-resonance experiments for sequential NMR assignments of large proteins. J Am Chem Soc 121:844–848
  • Salzmann M, Pervushin K, Wider G, Senn H, Wüthrich K. 2000. NMR assignment and secondary structure determination of an octameric 110 kDa protein using TROSY in triple resonance experiments. J Am Chem Soc 122:7543–7548
  • Schaffner W, Weissmann C. 1973. Rapid, sensitive and specific method for determination of protein in dilute solution. Anal Biochem 56:502–514
  • Shukla HD, Vaitiekunas P, Cotter RJ. 2012. Advances in membrane proteomics and cancer biomarker discovery: current status and future perspective. Proteomics 12:3085–3104
  • Skrisovska L, Schubert M, Allain FH. 2010. Recent advances in segmental isotope labeling of proteins: NMR applications to large proteins and glycoproteins. J Biomol NMR 46:51–65
  • Sobhanifar S, Reckel S, Junge F, Schwarz D, Kai L, Karbyshev M, et al. 2010. Cell-free expression and stable isotope labelling strategies for membrane proteins. J Biomol NMR 46:33–43
  • Spooner PR, Rutherford NG, Watts A, Henderson PJ. 1994. NMR observation of substrate in the binding-site of an active sugar-H+ symport protein in native membranes. Proc Natl Acad Sci USA 91:3877–3881
  • Sun L, Zeng X, Yan C, Sun X, Gong X, Rao Y, Yan N. 2012. Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature 490:361–366
  • Takeda M, Ono AM, Terauchi T, Kainosho M. 2010. Application of SAIL phenylalanine and tyrosine with alternative isotope-labeling patterns for protein structure determination. J Biomol NMR 46:45–49
  • Thorens B, Mueckler M. 2010. Glucose transporters in the 21st century. Am J Physiol Endocrinol Metab 298:E141–E145
  • Trbovic N, Klammt C, Koglin A, Löhr F, Bernhard F, Dötsch V. 2005. Efficient strategy for the rapid backbone assignment of membrane proteins. J Am Chem Soc 127:13504–13505
  • Tugarinov V, Hwang PM, Ollerenshaw JE, Kay LE. 2003. Cross-correlated relaxation enhanced 1H-13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. J Am Chem Soc 125:10420–10428
  • Tugarinov V, Kay LE. 2003. Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods. J Am Chem Soc 125:13868–13878
  • Tugarinov V, Kay LE. 2004a. Stereospecific NMR assignments of prochiral methyls, rotameric states and dynamics of valine residues in malate synthase G. J Am Chem Soc 126:9827–9836
  • Tugarinov V, Kay LE. 2004b. An isotope labeling strategy for methyl-TROSY spectroscopy. J Biomol NMR 28:165–172
  • Tugarinov V, Sprangers R, Kay LE. 2004. Line narrowing in methyl-TROSY using zero-quantum 1H-13C NMR spectroscopy. J Am Chem Soc 126:4921–4925
  • Venters RA, Thompson R, Cavanagh J. 2002. Current approaches for the study of large proteins by NMR. J Mol Struct 602:275–292
  • von Heijne G. 2007. The membrane protein universe: what’s out there and why bother? J Int Med 261:543–557
  • Wallin E, von Heijne G. 1998. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Prot Sci 7:1029–1038
  • Walmsley AR, Lowe AG, Henderson PJ. 1994a. The kinetics and thermodynamics of the binding of cytochalasin B to sugar transporters. Eur J Biochem 221:513–522
  • Walmsley AR, Martin GE, Henderson PJ. 1994b. 8-Anilino-1-naphthalenesulfonate is a fluorescent probe of conformational changes in the D-galactose-H+ symport protein of Escherichia coli. J Biol Chem 269:17009–17019
  • Ward A, Sanderson NM, O’Reilly J, Rutherford NG, Poolman B, Henderson PJ. 2000. The amplified expression, identification, purification, assay and properties of hexahistidine-tagged bacterial membrane transport proteins. In Baldwin SA, ed. Membrane transport – a practical approach. Oxford: Blackwell, 141–166
  • Watanabe H, Koopmann TT, Scouarnec SL, Yang T, Ingram CR, Schott J-J, et al. 2008. Sodium channel b1subunit mutations associated with Brugada syndrome and cardiac conduction disease in humans. J Clin Invest 118:2260–2268
  • Wider G, Wüthrich K. 1999. NMR spectroscopy of large molecules and multimolecular assemblies in solution. Curr Opin Struct Biol 9:594–601
  • Yang D, Kay LE. 1999. TROSY triple-resonance four-dimensional NMR spectroscopy of a 46 ns tumbling protein. J Am Chem Soc 121:2571–2575
  • Yu L, Sun C, Song D, Shen J, Xu N, Gunasekera A, et al. 2005. Nuclear magnetic resonance structural studies of a potassium channel-charybdotoxin complex. Biochemistry 44:15834–15841

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.