Multiple protonation states of vesicular acetylcholine transporter detected by binding of [3H]vesamicol

Biochemistry

Volumn 48, Issue 38, 2009, Pages 8965-8975

  Khare, Parul ^a   White, Aubrey R ^a   Parsons, Stanley M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC PH; ALKALINE PH; ALKYLAMINE; ALLOSTERIC SITE; BINDING DATA; BIPHASIC; CYCLOHEXANOL; DISSOCIATION CONSTANT; EQUILIBRIUM SATURATION; HIGH PH; LONG TERM EXPOSURE; NEUTRAL PH; POSITIVELY CHARGED; PRE-EXPOSURE; PROTONATED; PROTONATION STATE; TIME-DEPENDENT;

AMINES; ASSAYS; BINDING ENERGY; BINDING SITES; DEPROTONATION; DISSOCIATION; PROTONS;

PH EFFECTS;

TRITIUM; VESAMICOL; VESICULAR ACETYLCHOLINE TRANSPORTER; PIPERIDINE DERIVATIVE; PROTON; RECOMBINANT PROTEIN; SLC18A3 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; DISSOCIATION CONSTANT; DRUG BINDING; DRUG BINDING SITE; NONHUMAN; PH; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTON TRANSPORT; RAT; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; ANIMAL; BINDING COMPETITION; BINDING SITE; CELL STRAIN; CHEMICAL MODEL; CHEMISTRY; DRUG ANTAGONISM; ENZYME STABILITY; GENETICS; HUMAN; IN VITRO STUDY; KINETICS; METABOLISM;

ALLOSTERIC SITE; ANIMALS; BINDING, COMPETITIVE; ENZYME STABILITY; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, CHEMICAL; PC12 CELLS; PIPERIDINES; PROTONS; RATS; RECOMBINANT PROTEINS; TRITIUM; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 70349785768     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900759v     Document Type: Article

References (52)

1. Parsons, S. M., Prior, C., and Marshall, I. G. (1993) Acetylcholine transport, storage, and release. Int. Rev. Neurobiol. 35, 279-390.
2. Usdin, T. B., Eiden, L. E., Bonner, T. I., and Erickson, J. D. (1995) Molecular biology of the vesicular ACh transporter. Trends Neurosci. 18, 218-224.
3. Saier, M. H. J., Beatty, J. T., Goffeau, A., Harley, K. T., Heijne, W. H., Huang, S. C., Jack, D. L., Jahn, P. S., Lew, K., Liu, J., Pao, S. S., Paulsen, I. T., Tseng, T. T., and Virk, P. S. (1999) The major facilitator superfamily. J. Mol. Microbiol. Biotechnol. 1, 257-279
4. 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)
5. 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)
6. Hirai, T., Heymann, J. A. W., Shi, D., Sarker, R., Maloney, P. C., and Subramaniam, S. (2002) Three-dimensional structure of a bacterial oxalate transporter. Nat. Struct. Mol. Biol. 9, 597-600.
7. 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.
8. Law, C. J., Maloney, P. C., and Wang, D. N. (2008) Ins and outs of major facilitator superfamily antiporters. Annu. Rev. Microbiol. 62, 289-305.
9. Vardy, E., Arkin, I. T., Gottschalk, K. E., Kaback, H. R., and Schuldiner, S. (2004) Structural conservation in the major facilitator superfamily as revealed by comparative modeling. Protein Sci. 13, 1832-1840. (Pubitemid 38822121)
10. Nguyen, M. L., Cox, G. D., and Parsons, S. M. (1998) Kinetic parameters for the vesicular acetylcholine transporter: two protons are exchanged for one acetylcholine. Biochemistry 37, 13400-13410.
11. Bahr, B. A., and Parsons, S. M. (1986) Acetylcholine transport and drug inhibition kinetics in Torpedo synaptic vesicles. J. Neurochem. 46, 1214-1218.
12. Bravo, D. T., Kolmakova, N. G., and Parsons, S. M. (2005) Mutational and pH analysis of ionic residues in transmembrane domains of vesicular acetylcholine transporter. Biochemistry 44, 7955-7966.
13. Kim, M. H., Lu, M., Lim, E. J., Chai, Y. G., and Hersh, L. B. (1999) Mutational analysis of aspartate residues in the transmembrane regions and cytoplasmic loops of rat vesicular acetylcholine transporter. J. Biol. Chem. 274, 673-680.
14. Ojeda, A. M., Kolmakova, N. G., and Parsons, S. M. (2004) Acetylcholine binding site in the vesicular acetylcholine transporter. Biochemistry 43, 11163-11174. (Pubitemid 39180360)
15. D'rozario, R. S. G., and Sansom, M. S. P. (2008) Helix dynamics in a membrane transport protein: comparative simulations of the glycerol-3-phosphate transporter and its constituent helices. Mol. Membr. Biol. 25, 571-583.
16. Kornreich, W. D., and Parsons, S. M. (1988) Sidedness and chemical and kinetic properties of the vesamicol receptor of cholinergic synaptic vesicles. Biochemistry 27, 5262-5267.
17. Dixon, M., and Webb, E. C. (1964) Enzymes , pp 128-145, Longmans, London.
18. Rogers, G. A., Parsons, S. M., Anderson, D. C., Nilsson, L. M., Bahr, B. A., Kornreich, W. D., Kaufman, R., Jacobs, R. S., and Kirtman, B. (1989) Synthesis, in vitro acetylcholine-storage-blocking activities, and biological properties of derivatives and analogues of trans-2-(4-phenylpiperidino) cyclohexanol (vesamicol). J. Med. Chem. 32, 1217-1230. (Pubitemid 19149973)
19. a of vesamicol, unpublished work.
20. Shimojo, M., Wu, D., and Hersh, L. B. (1998) The cholinergic gene locus is coordinately regulated by protein kinase A II in PC12 cells. J. Neurochem. 71, 1118-1126. (Pubitemid 28390265)
21. Bonzelius, F., Herman, G., Cardone, M., Mostov, K., and Kelly, R. (1994) The polymeric immunoglobulin receptor accumulates in specialized endosomes but not synaptic vesicles within the neurites of transfected neuroendocrine PC12 cells. J. Cell Biol. 127, 1603-1616. (Pubitemid 24380899)
22. Khare, P., White, A. R., Mulakaluri, A., and Parsons, S. M. (2009) Equilibrium binding and transport characterization of vesicular acetylcholine transporter, Methods Mol. Biol. (in press).
23. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
24. Varoqui, H., and Erickson, J. D. (1996) Active transport of acetylcholine by the human vesicular acetylcholine transporter. J. Biol. Chem. 271, 27229-27232.
25. Keller, J. E., and Parsons, S. M. (2000) A critical histidine in the vesicular acetylcholine transporter. Neurochem. Int. 36, 113-117.
26. Rogers, G. A., Kornreich, W. D., Hand, K., and Parsons, S. M. (1993) Kinetic and equilibriumcharacterization of vesamicol receptor ligand complexes with picomolar dissociation constants. Mol. Pharmacol. 44, 633-641.
27. Efange, S. M., Mach, R. H., Smith, C. R., Khare, A. B., Foulon, C., Akella, S. K., Childers, S. R., and Parsons, S. M. (1995) Vesamicol analogues as sigma ligands. Molecular determinants of selectivity at the vesamicol receptor. Biochem. Pharmacol. 49, 791-797.
28. Sagi, N., Yamamoto, H., Yamamoto, T., Okuyama, S., and Moroji, T. (1996) Possible expression of a σ1 site in rat pheochromocytoma (PC12) cells. Eur. J. Pharmacol. 304, 185-190.
29. Compute pI/Mw tool.http://ca.expasy.org/tools/pi-tool.html, accessed Feb 5, 2009.
30. Szakács, Z., Kraszni, M., and Noszál, B. (2004) Determination of microscopic acid-base parameters from NMR-pH titrations. Anal. Bioanal. Chem. 378, 1428-1448.
31. 13CNMR. Tetrahedron 52, 5319-5338.
32. Brocklehurst, K. (1994) A sound basis for pH-dependent kinetic studies on enzymes. Protein Eng. 7, 291-299. (Pubitemid 24063127)
33. Josée, E., Leysen, and Gommeren, W. (1986) Drug-receptor dissociation time, new tool for drug research: Receptor binding affinity and drug-receptor dissociation profiles of serotonin, dopamine, histamine, antagonists, and opiates. Drug Dev. Res. 8, 119-131.
34. Zhu, H., Duerr, J. S., Varoqui, H., McManus, J. R., Rand, J. B., and Erickson, J. D. (2001) Analysis of point mutants in the Caenorhabditis elegans vesicular acetylcholine transporter reveals domains involved in substrate translocation. J. Biol. Chem. 276, 41580-41587.
35. Khare, P., Ojeda, A. M., Chandrasekaran, A., and Parsons, S. M. (2007) Interacting acidic residues in transmembrane segments of vesicular acetylcholine transporter, Poster abstract 579.18/M27, Society for Neuroscience Conference, San Diego.
36. Kim, M. H., Lu, M., Kelly, M., and Hersh, L. B. (2000) Mutational analysis of basic residues in the rat vesicular acetylcholine transporter. Identification of a transmembrane ion pair and evidence that histidine is not involved in proton translocation. J. Biol. Chem. 275, 6175-6180.
37. Merickel, A., Kaback, H. R., and Edwards, R. H. (1997) Charged residues in transmembrane domains II and XI of a vesicular monoamine transporter form a charge pair that promotes high affinity substrate recognition. J. Biol. Chem. 272, 5403-5408.
38. Bahr, B. A., Clarkson, E. D., Rogers, G. A., Noremberg, K., and Parsons, S. M. (1992) A kinetic and allosteric model for the acetylcholine transporter-vesamicol receptor in synaptic vesicles. Biochemistry 31, 5752-5762.
39. Volkow, N. D., Ding, Y.-S., Fowler, J. S., and Gatley, S. J. (2001) Imaging brain cholinergic activity with positron emission tomography: its role in the evaluation of cholinergic treatments in Alzheimer's dementia. Biol. Psychiat. 49, 211-220.
40. Langer, O., and Halldin, C. (2002) PET and SPET tracers for mapping the cardiac nervous system. Eur. J. Nucl. Med. Mol. I 29, 416-434.
41. 18F-labeled positron emission tomography (PET) ligands for imaging the vesicular acetylcholine transporter. J. Med. Chem. 52, 1358-1369.
42. Ingvar, M., Stone-Elander, S., Rogers, G. A., Johansson, B., Eriksson, L., Parsons, S. M., and Widen, L. (1993) Striatal D2/acetylcholine interactions: PET studies of the vesamicol receptor. NeuroReport 4, 1311-1314. (Pubitemid 23297977)
43. Efange, S. M. N., Langason, R. B., and Khare, A. B. (1996) Agerelated diminution of dopamine antagonist-stimulated vesamicol receptor binding. J. Nucl. Med. 37, 1192-1197.
44. Holden, J. E., and Doudet, D. J. (2004) Positron emission tomography receptor assay with multiple ligand concentrations: an equilibrium approach. Methods Enzymol. 385 (Imaging Biol. Res., Part A), 169-184.
45. + compartmentation and cellular regulation during hypoxic/ischemic conditions. Neurochem. Res. 25, 1385-1396.
46. Grafe, P. (1998) Abnormal cytoplasmic pH in diseases of nerve and muscle, in pH and Brain Function (Kaila, K., and Ransom, B. R., Eds.) pp 621-628, Wiley-Liss, New York.
47. a value of 9.02 ± 0.40 for (±)-vesamicol and 8.27 ± 0.40 for (±)-ABV as estimated by Advanced Chemistry Development using Software V8.14 for Solaris (1994-2009 by ACD/Laboratories).
48. Parsons, S. M. (2000) Transport mechanisms in acetylcholine and monoamine storage. FASEB J. 14, 2423-2434.
49. Scherman, D., and Henry, J. (1983) The catecholamine carrier of bovine chromaffin granules. Form of the bound amine. Mol. Pharmacol. 23, 431-436.
50. Scherman, D. H., and Henry, Jean Pierre (1982) Acid-base properties of the catecholamine uptake inhibitors tetrabenazine and dihydrotetrabenazine. Biochimie 64, 915-921.
51. Brooks, D. J., Frey, K. A., Marek, K. L., Oakes, D., Paty, D., Prentice, R., Shults, C. W., and Stoessl, A. J. (2003) Assessment of neuroimaging techniques as biomarkers of the progression of Parkinson's disease. Exp. Neurol. 184 (Suppl. 1), S68-S79.
52. Ravina, B., Eidelberg, D., Ahlskog, J. E., Albin, R. L., Brooks, D. J., Carbon, M., Dhawan, V., Feigin, A., Fahn, S., Guttman, M., Gwinn-Hardy, K., McFarland, H., Innis, R., Katz, R. G., Kieburtz, K., Kish, S. J., Lange, N., Langston, J. W., Marek, K., Morin, L., Moy, C., Murphy, D., Oertel, W. H., Oliver, G., Palesch, Y., Powers, W., Seibyl, J., Sethi, K. D., Shults, C. W., Sheehy, P., Stoessl, A. J., and Holloway, R. (2005) The role of radiotracer imaging in Parkinson disease. Neurology 64, 208-215.