A numbering system for MFS transporter proteins

Frontiers in Molecular Biosciences

Volumn 3, Issue JUN, 2016, Pages

  Lee, Joanna ^a   Sands, Zara A ^b   Biggin, Philip C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UCB PHARMA   (Belgium)

Author keywords

Alternating access; Homology modeling; LacY; Transmembrane; Transport

Indexed keywords

EID: 84992456610     PISSN: None     EISSN: 2296889X     Source Type: Journal    
DOI: 10.3389/fmolb.2016.00021     Document Type: Article

References (54)

1. Almaula, N., Ebersole, B. J., Ballesteros, J. A., Weinstein, H., and Sealfon, S. C. (1996). Contribution of a helix 5 locus to selectivity of hallucinogenic and nonhallucinogenic ligands for the human 5-hydroxytryptamine2A and 5-hydroxytryptamine2C receptors: direct and indirect effects on ligand affinity mediated by the same locus. Mol. Pharmacol. 50, 34-42
2. Baker, D., and Sali, A. (2001). Protein structure prediction and structural genomics. Science 294, 93-96. doi: 10.1126/science.1065659
3. Burckhardt, G., and Wolff, N. A. (2000). Structure of renal organic anion and cation transporters. Am. J. Physiol. Renal Physiol. 278, F853-F866
4. Chiang, Z., Vastermark, A., Punta, M., Coggill, P. C., Mistry, J., Finn, R. D., et al. (2015). The complexity, challenges and benefits of comparing two transporter classification systems in TCDB and Pfam. Brief. Bioinform. 16, 865-872. doi: 10.1093/bib/bbu053
5. Devineni, D., Vaccaro, N., Murphy, J., Curtin, C., Mamidi, R. N. V. S., Weiner, S., et al. (2015). Effects of rifampin, cyclosporine A, and probenecid on the pharmacokinetic profile of canagliflozin, a sodium glucose co-transporter 2 inhibitor, in healthy participants. Int. J. Clin. Pharmacol. Ther. 53, 115-128. doi: 10.5414/CP202158
6. Doki, S., Kato, H. E., Solcan, N., Iwaki, M., Koyama, M., Hattori, M., et al. (2013). Structural basis for dynamic mechanism of proton-coupled symport by the peptide transporter POT. Proc. Natl. Acad. Sci. U.S.A. 110, 11343-11348. doi: 10.1073/pnas.1301079110
7. Edgar, R. C. (2004a). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. doi: 10.1093/nar/gkh340
8. Edgar, R. C. (2004b). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. doi: 10.1186/1471-2105-5-113
9. Eraly, S. (2008). Implications of the alternating access model for organic anion transporter kinetics. J. Membr. Biol. 226, 35-42. doi: 10.1007/s00232-008-9137-1
10. Eyre, T. A., Partridge, L., and Thornton, J. M. (2004). Computational analysis of α-helical membrane protein structure: implications for the prediction of 3D structural models. Prot. Eng. Des. Sel. 17, 613-624. doi: 10.1093/protein/gzh072
11. Finn, R. D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R. Y., Eddy, S. R., et al. (2014). Pfam: the protein families database. Nucl. Acids Res. 42, D222-D230. doi: 10.1093/nar/gkt1223
12. Giboureau, N., Som, I. M., Boucher-Arnold, A., Guilloteau, D., and Kassiou, M. (2010). PET radioligands for the Vesicular Acetylcholine Transporter (VAChT). Curr. Top. Med. Chem. 10, 1569-1583. doi: 10.2174/156802610793176846
13. Guan, L., and Kaback, H. R. (2006). Lessons from lactose permease. Annu. Rev. Biophys. Biomol. Struct. 35, 67-91. doi: 10.1146/annurev.biophys.35.040405.102005
14. Hinoi, E., Takarada, T., Tsuchihashi, Y., and Yoneda, Y. (2005). Glutamate transporters as drug targets. Curr. Drug Targets CNS Neurol. Disord. 4, 211-220. doi: 10.2174/1568007053544093
15. Humphrey, W., Dalke, A., and Schulten, K. (1996). VMD-Visual molecular dynamics. J. Mol. Graph. 14, 33-38. doi: 10.1016/0263-7855(96)00018-5
16. Isberg, V., de Graaf, C., Bortolato, A., Cherezov, V., Katritch, V., Marshall, F. H., et al. (2015). Generic GPCR residue numbers-aligning topology maps while minding the gaps. Trends Pharm. Sci. 36, 22-31. doi: 10.1016/j.tips.2014.11.001
17. Javitch, J. A., Ballesteros, J. A., Weinstein, H., and Chen, J. (1998). A cluster of aromatic residues in the sixth membrane-spanning segment of the dopamine D2 receptor is accessible in the binding-site crevice. Biochemistry 37, 998-1006. doi: 10.1021/bi972241y
18. Kaback, H. R., Smirnova, I., Kasho, V., Nie, Y., and Zhou, Y. (2011). The alternating access transport mechanism in LacY. J. Membr. Biol. 239, 85-93. doi: 10.1007/s00232-010-9327-5
19. Kasho, V. N., Smirnova, I. N., and Kaback, H. R. (2006). Sequence alignment and homology threading reveals prokaryotic and eukaryotic proteins similar to lactose permease. J. Mol. Biol. 358, 1060-1070. doi: 10.1016/j.jmb.2006.02.049
20. Keller, R., Ziegler, C., and Schneider, D. (2014). When two turn into one: evolution of membrane transporters from half modules. Biol. Chem. 395, 1379-1388. doi: 10.1515/hsz-2014-0224
21. Klitgaard, H., Matagne, A., Gobert, J., and Wülfert, E. (1998). Evidence for a unique profile of levetiracetam in rodent models of seizures and epilepsy. Eur. J. Pharmacol. 353, 191-206. doi: 10.1016/S0014-2999(98)00410-5
22. Lin, L., Yee, S. W., Kim, R. B., and Giacomini, K. M. (2015). SLC transporters as therapeutic targets: emerging opportunities. Nat. Rev. Drug. Discov. 14, 543-560. doi: 10.1038/nrd4626
23. Lomize, M. A., Lomize, A. L., Pogozheva, I. D., and Mosberg, H. I. (2006). OPM: Orientations of protetins in membranes database. Bioinformatics 22, 623-625. doi: 10.1093/bioinformatics/btk023
24. Löscher, W., Hönack, D., and Rundfeldt, C. (1998). Antiepileptogenic effects of the novel anticonvulsant levetiracetam (ucb l059) in the kindling model of temporal lobe epilepsy. J. Pharmacol. Exp. Ther. 284, 474-479
25. Lynch, B. A., Lambeng, N., Nocka, K., Kensel-Hammes, P., Bajjalieh, S. M., Matagne, A., et al. (2004). The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc. Natl. Acad. Sci. U.S.A. 101, 9861-9866. doi: 10.1073/pnas.0308208101
26. Madej, M. G. (2015). "Comparative sequence-function analysis of the major facilitator superfamily: the mix-and-match method, Chap. 24". in Methods Enzymol, ed K. S. Arun (Academic Press) 557, 521-549. doi: 10.1016/bs.mie.2014.12.015
27. Madej, M. G., Dang, S., Yan, N., and Kaback, H. R. (2013). Evolutionary mix-and-match with MFS transporters. Proc. Natl. Acad. Sci. U.S.A. 110, 5870-5874. doi: 10.1073/pnas.1303538110
28. Madej, M. G., and Kaback, H. R. (2013). Evolutionary mix-and-match with MFS transporters II. Proc. Natl. Acad. Sci. U.S.A. 110, E4831-E4838. doi: 10.1073/pnas.1303538110
29. Madej, M. G., Sun, L., Yan, N., and Kaback, H. R. (2014). Functional architecture of MFS d-glucose transporters. Proc. Natl. Acad. Sci. U.S.A. 111, E719-E727. doi: 10.1073/pnas.1400336111
30. Marger, M. D., and Saier, M. H. (1993). A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem. Sci. 18, 13-20. doi: 10.1016/0968-0004(93)90081-W
31. Masureel, M., Martens, C., Stein, R. A., Mishra, S., Ruysschaert, J.-M., McHaourab, H. S., et al. (2014). Protonation drives the conformational switch in the multidrug transporter LmrP. Nat. Chem. Biol. 10, 149-155. doi: 10.1038/nchembio.1408
32. Newstead, S., Drew, D., Cameron, A. D., Postis, V. L. G., Xia, X., Fowler, P. W., et al. (2011). Crystal structure of a prokaryotic homologue of the mammalian oligopeptide-proton symporters, PepT1 and PepT2. EMBO J. 30, 417-426. doi: 10.1038/emboj.2010.309
33. Pao, S. S., Paulsen, I. T., and Saier, M. H. (1998). Major Facilitator Superfamily. Microbiol. Mol. Biol. Rev. 62, 1-34
34. Pascual, J. M., Wang, D., Yang, R., Shi, L., Yang, H., and De Vivo, D. C. (2008). Structural signatures and membrane helix 4 in GLUT1: Inferences from human blood-brain glucose transport mutants. J. Biol. Chem. 283, 16732-16742. doi: 10.1074/jbc. M801403200
35. Paulsen, I. T., Brown, M. H., and Skurray, R. A. (1996). Proton-dependent multidrug efflux systems. Microb. Rev. 60, 575-608
36. Pazdernik, N. J., Cain, S. M., and Brooker, R. J. (1997). An analysis of suppressor mutations suggests that the two halves of the lactose permease function in a symmetrical manner. J. Biol. Chem. 272, 26110-26116. doi: 10.1074/jbc.272.42.26110
37. Radestock, S., and Forrest, L. R. (2011). The alternating-access mechanism of MFS transporters arises from inverted-topology repeats. J. Mol. Biol. 407, 698-715. doi: 10.1016/j.jmb.2011.02.008
38. Reddy, V. S., Shlykov, M. A., Castillo, R., Sun, E. I., and Saier, M. H. (2012). The major facilitator superfamily (MFS) revisited. FEBS J. 279, 2022-2035. doi: 10.1111/j.1742-4658.2012.08588.x
39. Ren, Q., Kang, K. H., and Paulsen, I. T. (2004). TransportDB: a relational database of cellular membrane transport systems. Nucl. Acids Res. 32, D284-D288. doi: 10.1093/nar/gkh016
40. Rost, B. (1999). Twilight zone of protein sequence alignments. Prot. Eng. 12, 85-94
41. Saier, M. H. Jr., and Paulsen, I. T. (2001). Phylogeny of multidrug transporters. Semin. Cell Dev. Biol. 12, 205-213. doi: 10.1006/scdb.2000.0246
42. Saier, M. H. Jr., Reddy, V. S., Tamang, D. G., and Västermark, Å. (2014). The transporter classification database. Nucl. Acids Res. 42, D251-D258. doi: 10.1093/nar/gkt1097
43. Shi, Y. (2013). Common folds and transport mechanisms of secondary active transporters. Annu. Rev. Biophys. 42, 51-72. doi: 10.1146/annurev-biophys-083012-130429
44. Smirnova, I., Kasho, V., and Kaback, H. R. (2011). Lactose permease and the alternating access mechanism. Biochemistry 50, 9684-9693. doi: 10.1021/bi2014294
45. Smirnova, I., Kasho, V., and Kaback, H. R. (2014). Real-time conformational changes in LacY. Proc. Natl. Acad. Sci. U.S.A. 111, 8440-8445. doi: 10.1073/pnas.1408374111
46. Suzek, B. E., Huang, H., McGarvey, P., Mazumder, R., and Wu, C. H. (2007). UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23, 1282-1288. doi: 10.1093/bioinformatics/btm098
47. Tramontano, A. (1998). Homology modeling with low sequence identity. Methods 14, 293-300. doi: 10.1006/meth.1998.0585
48. Västermark, Å., and Saier, M. H. (2014). Major Facilitator Superfamily (MFS) evolved without 3-transmembrane segment unit rearrangements. Proc. Natl. Acad. Sci. U.S.A. 111, E1162-E1163. doi: 10.1073/pnas.1400016111
49. Venkatakrishnan, A. J., Deupi, X., Lebon, G., Tate, C. G., Schertler, G. F., and Babu, M. M. (2013). Molecular signatures of G-protein-coupled receptors. Nature 494, 185-194. doi: 10.1038/nature11896
50. von Heijne, G. V. (1992). Membrane protein structure prediction. Hydrophobicity analysis and the positive inside rule. J. Mol. Biol. 225, 487-494. doi: 10.1016/0022-2836(92)90934-C
51. Yaffe, D., Radestock, S., Shuster, Y., Forrest, L. R., and Schuldiner, S. (2013). Identification of molecular hinge points mediating alternating access in the vesicular monoamine transporter VMAT2. Proc. Natl. Acad. Sci. U.S.A. 110, E1332-E1341. doi: 10.1073/pnas.1220497110
52. Yan, N. (2015). Structural biology of the major facilitator superfamily transporters. Annu. Rev. Biophys. 44, 257-283. doi: 10.1146/annurev-biophys-060414-033901
53. Yan, N. (2016). Structural advances for the major facilitator superfamily (MFS) transporters. Trends Biochem. Sci. 38, 151-159. doi: 10.1016/j.tibs.2013.01.003
54. Zhou, W., Flanagan, C., Ballesteros, J. A., Konvicka, K., Davidson, J. S., Weinstein, H., et al. (1994). A reciprocal mutation supports helix 2 and helix 7 proximity in the gonadotropin-releasing hormone receptor. Mol. Pharmacol. 45, 165-170