Combining modelling and mutagenesis studies of synaptic vesicle protein 2A to identify a series of residues involved in racetam binding

Biochemical Society Transactions

Volumn 39, Issue 5, 2011, Pages 1341-1347

  Shi, Jiye ^a   Anderson, Dina ^a,b   Lynch, Berkley A ^a,c   Castaigne, Jean Gabriel ^a,d   Foerch, Patrik ^a   Lebon, Florence ^a  

^a UCB PHARMA   (Belgium)

^b MEDIMMUNE   (United States)

^c Link Medicine   (United States)

^d Napp Pharmaceuticals   (United Kingdom)

Author keywords

Epilepsy; Homology modelling; Mutagenesis; Racetam binding; Synaptic vesicle protein 2A (SV2A)

Indexed keywords

ACETAMIDE; ALANINE; ETIRACETAM; ETIRACETAM DERIVATIVE; IMIDAZOLE; ISOLEUCINE; MAJOR FACILITATOR SUPERFAMILY; ORGANIC ANION TRANSPORTER 1; ORGANIC CATION TRANSPORTER 1; ORGANIC CATION TRANSPORTER 2; PROTEIN; SYNAPTIC VESICLE PROTEIN 2A; UNCLASSIFIED DRUG;

ALGORITHM; BINDING AFFINITY; CONFERENCE PAPER; DRUG PROTEIN BINDING; LIGAND BINDING; MOLECULAR DOCKING; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SYNAPSE VESICLE;

ALANINE; AMINO ACID SEQUENCE; ANIMALS; ANTICONVULSANTS; BINDING SITES; HUMANS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; PIRACETAM; PROTEIN BINDING; RATS; SEQUENCE ALIGNMENT;

ANIMALIA;

EID: 80053381169     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0391341     Document Type: Conference Paper

References (44)

1. Scheuer, M.L. and Pedley, T.A. (1990) The evaluation and treatment of seizures. N. Engl. J. Med. 323, 1468-1474 (Pubitemid 20384956)
2. 3H]ucb 30889 to levetiracetam binding sites in rat brain. Eur. J. Pharmacol. 478, 1-9
3. Von Rosenstiel, P. (2007) Brivaracetam (UCB 34714). Neurotherapeutics 4, 84-87
4. Kaminski, R.M., Matagne, A., Patsalos, P.N. and Klitgaard, H. (2009) Benefit of combination therapy in epilepsy: a review of the preclinical evidence with levetiracetam. Epilepsia 50, 387-397
5. Noyer, M., Gillard, M., Matagne, A., Hénichart, J.-P. and Wülfert, E. (1995) The novel antiepileptic drug levetiracetam (ucb L059) appears to act via a specific binding site in CNS membranes. Eur. J. Pharmacol. 286, 137-146
6. Fuks, B., Gillard, M., Michel, P., Lynch, B.A., Vertongen, P., Leprince, P., Klitgaard, H. and Chatelain, P. (2003) Localisation and photoaffinity labelling of the levetiracetam binding site in rat brain and certain cell lines. Eur. J. Pharmacol. 478, 11-19 (Pubitemid 38366069)
7. Lynch, B.A., Lambeng, N., Nocka, K., Kensel-Hammes, P., Bajjalieh, S.M., Matagne, A. and Fuks, B. (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 (Pubitemid 38869327)
8. Gillard, M., Chatelain, P. and Fuks, B. (2006) Binding characteristics of levetiracetam to synaptic vesicle protein 2A (SV2A) in human brain and in CHO cells expressing the human recombinant protein. Eur. J. Pharmacol. 536, 102-108
9. Bajjalieh, S.M., Frantz, G.D., Weimann, J.M., McConnell, S.K. and Scheller, R.H. (1994) Differential expression of synaptic vesicle protein 2 (SV2) isoforms. J. Neurosci. 14, 5223-5235 (Pubitemid 24279045)
10. Bajjalieh, S.M., Peterson, K., Linial, M. and Scheller, R.H. (1993) Brain contains two forms of synaptic vesicle protein 2. Proc. Natl. Acad. Sci. U.S.A. 90, 2150-2154 (Pubitemid 23078583)
11. Buckley, K. and Kelly, R.B. (1985) Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J. Cell Biol. 100, 1284-1294 (Pubitemid 15093481)
12. Bajjalieh, S.M., Peterson, K., Shinghal, R. and Scheller, R.H. (1992) SV2, a brain synaptic vesicle protein homologous to bacterial transporters. Science 257, 1271-1273
13. Reference deleted
14. Abramson, J., Smirnova, I., Kasho, V., Verner, G., Kaback, H.R. and Iwata, S. (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301, 610-615 (Pubitemid 36927939)
15. Yin, Y., He, X., Szewczyk, P., Nguyen, T. and Chang, G. (2006) Structure of the multidrug transporter EmrD from Escherichia coli. Science 312, 741-744
16. Dang, S., Sun, L., Huang, Y., Lu, F., Liu, Y., Gong, H., Wang, J. and Yan, N. (2010) Structure of a fucose transporter in an outward-open conformation. Nature 467, 734-738
17. 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 (Pubitemid 36927940)
18. Newstead, S., Drew, D., Cameron, A.D., Postis, V.L., Xia, X., Fowler, P.W., Ingram, J.C., Carpenter, E.P., Sansom, M.S., McPherson, M.J. et al. (2011) Crystal structure of a prokaryotic homologue of the mammalian oligopeptide-proton symporters, PepT1 and PepT2. EMBO J. 30, 417-426
19. Cuthbertson, J.M., Doyle, D.A. and Sansom, M.S. (2005) Transmembrane helix prediction: a comparative evaluation and analysis. Protein Eng. Des. Sel. 18, 295-308 (Pubitemid 40942576)
20. Arai, M., Mitsuke, H., Ikeda, M., Xia, J.X., Kikuchi, T., Satake, M. and Shimizu, T. (2004) ConPred II: a consensus prediction method for obtaining transmembrane topology models with high reliability. Nucleic Acids Res. 32, W390-W393 (Pubitemid 38997365)
21. Taylor, P.D., Attwood, T.K. and Flower, D.R. (2003) BPROMPT: a consensus server for membrane protein prediction. Nucleic Acids Res. 31, 3698-3700 (Pubitemid 37442226)
22. Jones, D.T. (2007) Improving the accuracy of transmembrane protein topology prediction using evolutionary information. Bioinformatics 23, 538-544
23. Käll, L., Krogh, A. and Sonnhammer, E.L. (2005) An HMM posterior decoder for sequence feature prediction that includes homology information. Bioinformatics 21 (Suppl. 1), i251-i257 (Pubitemid 41794496)
24. Viklund, H. and Elofsson, A. (2004) Best α-helical transmembrane protein topology predictions are achieved using hidden Markov models and evolutionary information. Protein Sci. 13, 1908-1917 (Pubitemid 38822130)
25. Chen, C.P., Kernytsky, A. and Rost, B. (2002) Transmembrane helix predictions revisited. Protein Sci. 11, 2774-2791 (Pubitemid 35365245)
26. Chen, C.P. and Rost, B. (2002) State-of-the-art in membrane protein prediction. Appl. Bioinformatics 1, 21-35
27. Park, Y. and Helms, V. (2006) How strongly do sequence conservation patterns and empirical scales correlate with exposure patterns of transmembrane helices of membrane proteins? Biopolymers 83, 389-399 (Pubitemid 44683083)
28. Punta, M., Forrest, L.R., Bigelow, H., Kernytsky, A., Liu, J. and Rost, B. (2007) Membrane protein prediction methods. Methods 41, 460-474 (Pubitemid 46420423)
29. Hirokawa, T., Boon-Chieng, S. and Mitaku, S. (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378-379 (Pubitemid 28393805)
30. Mitaku, S., Hirokawa, T. and Tsuji, T. (2002) Amphiphilicity index of polar amino acids as an aid in the characterization of amino acid preference at membrane-water interfaces. Bioinformatics 18, 608-616 (Pubitemid 34521049)
31. Krogh, A., Larsson, B., Von Heijne, G. and Sonnhammer, E.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580 (Pubitemid 33032862)
32. Cao, B., Porollo, A., Adamczak, R., Jarrell, M. and Meller, J. (2006) Enhanced recognition of protein transmembrane domains with prediction-based structural profiles. Bioinformatics 22, 303-309 (Pubitemid 43205376)
33. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 (Pubitemid 24354800)
34. Shi, J., Blundell, T.L. and Mizuguchi, K. (2001) FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310, 243-257 (Pubitemid 32619966)
35. Jessen-Marshall, A.E., Paul, N.J. and Brooker, R.J. (1995) The conserved motif, GXXX(D/E)(R/K)XG[X](R/K)(R/K), in hydrophilic loop 2/3 of the lactose permease. J. Biol. Chem. 270, 16251-16257
36. Pao, S.S., Paulsen, I.T. and Saier, Jr, M.H. (1998) Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62, 1-34 (Pubitemid 28130794)
37. Saier, Jr, M.H., Beatty, J.T., Goffeau, A., Harley, K.T., Heijne, W.H., Huang, S.C., Jack, D.L., Jahn, P.S., Lew, K., Liu, J. et al. (1999) The major facilitator superfamily. J. Mol. Microbiol. Biotechnol. 1, 257-279 (Pubitemid 129491947)
38. Kaback, H.R., Dunten, R., Frillingos, S., Venkatesan, P., Kwaw, I., Zhang, W. and Ermolova, N. (2007) Site-directed alkylation and the alternating access model for LacY. Proc. Natl. Acad. Sci. U.S.A. 104, 491-494 (Pubitemid 46123053)
39. Fiser, A. and Sali, A. (2003) Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol. 374, 461-491 (Pubitemid 37531821)
40. Sali, A. and Blundell, T.L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (Pubitemid 24007801)
41. Kwaw, I., Zen, K.C., Hu, Y. and Kaback, H.R. (2001) Site-directed sulfhydryl labeling of the lactose permease of Escherichia coli: helices IV and V that contain the major determinants for substrate binding. Biochemistry 40, 10491-10499 (Pubitemid 32816659)
42. Popp, C., Gorboulev, V., Muller, T.D., Gorbunov, D., Shatskaya, N. and Koepsell, H. (2005) Amino acids critical for substrate affinity of rat organic cation transporter 1 line the substrate binding region in a model derived from the tertiary structure of lactose permease. Mol. Pharmacol. 67, 1600-1611 (Pubitemid 40594159)
43. Gorboulev, V., Shatskaya, N., Volk, C. and Koepsell, H. (2005) Subtype-specific affinity for corticosterone of rat organic cation transporters rOCT1 and rOCT2 depends on three amino acids within the substrate binding region. Mol. Pharmacol. 67, 1612-1619 (Pubitemid 40594160)
44. 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