Structural and functional probing of the biogenic amine transporters by fluorescence spectroscopy

European Journal of Pharmacology

Volumn 479, Issue 1-3, 2003, Pages 13-22

  Rasmussen, Søren G F ^a   Adkins, Erika M ^a   Carroll, F Ivy ^b   Maresch, Martin J ^b   Gether, Ulrik ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b RTI INTERNATIONAL   (United States)

Author keywords

Biogenic amine; Flourescence spectroscopy; Functional probing; Structural probing

Indexed keywords

BIOGENIC AMINE; COCAINE; CYSTEINE; DOPAMINE; NORADRENALIN; RTI 233; SEROTONIN; SEROTONIN TRANSPORTER;

AMINE TRANSPORT; AMINO ACID TRANSPORT; DRUG BINDING; ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; INSECT CELL; MICELLE; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW;

EID: 0242660432     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2003.08.053     Document Type: Article

References (65)

1. Androutsellis-Theotokis A., Rudnick G. Accessibility and conformational coupling in serotonin transporter predicted internal domains. J. Neurosci. 22:2002;8370-8378.
2. Bacia K., Schwille P. A dynamic view of cellular processes by in vivo fluorescence auto- and cross-correlation spectroscopy. Methods. 29:2003;74-85.
3. Bonnet G., Krichevsky O., Libchaber A. Kinetics of conformational fluctuations in DNA hairpin-loops. Proc. Natl. Acad. Sci. 95:1998;8602-8606.
4. Carroll F.I., Lewin A.H., Kuhar M.J. Dopamine uptake blockers: structure-activity relationships. Reith M.E.A. Neurotransmitter Transporters: Structure, Function, and Regulation. 1997;263-295 Humana Press, Totowa, NJ.
5. Cha A., Bezanilla F. Characterizing voltage-dependent conformational changes in the Shaker K+ channel with fluorescence. Neuron. 19:1997;1127-1140.
6. Cha A., Snyder G.E., Selvin P.R., Bezanilla F. Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy. Nature. 402:1999;809-813.
7. Chang Y., Weiss D.S. Site-specific fluorescence reveals distinct structural changes with GABA receptor activation and antagonism. Nat. Neurosci. 5:2002;1163-1168.
8. Chattopadhyay K., Saffarian S., Elson E.L., Frieden C. Measurement of microsecond dynamic motion in the intestinal fatty acid binding protein by using fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. 99:2002;14171-14176.
9. Chen J.G., Rudnick G. Permeation and gating residues in serotonin transporter. Proc. Natl. Acad. Sci. 97:2000;1044-1049.
10. Chen N., Reith M.E. Structure and function of the dopamine transporter. Eur. J. Pharmacol. 405:2000;329-339.
11. Eggeling C., Fries J.R., Brand L., Gunther R., Seidel C.A. Monitoring conformational dynamics of a single molecule by selective fluorescence spectroscopy. Proc. Natl. Acad. Sci. 95:1998;1556-1561.
12. Ferrer J., Javitch J.A. Cocaine alters the accessibility of endogenous cysteines in putative extracellular and extracellular loops of the human dopamine transporter. Proc. Natl. Acad. Sci. 95:1998;9238-9243.
13. Gether U. Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr. Rev. 21:2000;90-113.
14. Gether U., Lin S., Kobilka B.K. Fluorescent labeling of purified beta2-adrenergic receptor: evidence for ligand-specific conformational changes. J. Biol. Chem. 270:1995;28268-28275.
15. Gether U., Lin S., Ghanouni P., Ballesteros J.A., Weinstein H., Kobilka B.K. Agonists induce conformational changes in transmembrane domains III and VI of the beta2 adrenoceptor. EMBO J. 16:1997;6737-6747.
16. Haga T., Haga K., Hulme E.C. Receptor Biochemistry: A Practical Approach. 1990;IRL Press, Oxford.
17. Hasler K., Panke O., Junge W. On the stator of rotary ATP synthase: the binding strength of subunit delta to (alpha beta)3 as determined by fluorescence correlation spectroscopy. Biochemistry. 38:1999;13759-13765.
18. Hastrup H., Karlin A., Javitch J.A. Symmetrical dimer of the human dopamine transporter revealed by cross-linking Cys-306 at the extracellular end of the sixth transmembrane segment. Proc. Natl. Acad. Sci. 98:2001;10055-10060.
19. Haustein E., Schwille P. Ultrasensitive investigations of biological systems by fluorescence correlation spectroscopy. Methods. 29:2003;153-166.
20. Hein L., Meinel L., Pratt R.E., Dzau V.J., Kobilka B.K. Intracellular trafficking of angiotensin II and its AT1 and AT2 receptors: evidence for selective sorting of receptor and ligand. Mol. Endocrinol. 11:1997;1266-1277.
21. Hess S.T., Huang S., Heikal A.A., Webb W.W. Biological and chemical applications of fluorescence correlation spectroscopy: a review. Biochemistry. 41:2002;697-705.
22. Iino R., Koyama I., Kusumi A. Single molecule imaging of green fluorescent proteins in living cells: E-cadherin forms oligomers on the free cell surface. Biophys. J. 80:2001;2667-2677.
23. Itokawa M., Lin Z., Cai N.S., Wu C., Kitayama S., Wang J.B., Uhl G.R. Dopamine transporter transmembrane domain polar mutants: DeltaG and DeltaDeltaG values implicate regions important for transporter functions. Mol. Pharmacol. 57:2000;1093-1103.
24. Jensen A.D., Guarnieri F., Rasmussen S.G., Asmar F., Ballesteros J.A., Gether U. Agonist-induced conformational changes at the cytoplasmic side of TM 6 in the {beta}2 adrenergic receptor mapped by site-selective fluorescent labeling. J. Biol. Chem. 276:2001;9279-9290.
25. Kastner C.N., Prummer M., Sick B., Renn A., Wild U.P., Dimroth P. The citrate carrier CitS probed by single-molecule fluorescence spectroscopy. Biophys. J. 84:2003;1651-1659.
26. Kilic F., Rudnick G. Oligomerization of serotonin transporter and its functional consequences. Proc. Natl. Acad. Sci. 97:2000;3106-3111.
27. Kitayama S., Shimada S., Xu H., Markham L., Donovan D.M., Uhl G.R. Dopamine transporter site-directed mutations differentially alter substrate transport and cocaine binding. Proc. Natl. Acad. Sci. 89:1992;7782-7785.
28. Kobilka B.K., Gether U. Use of fluorescence spectroscopy to study conformational changes in the beta 2-adrenoceptor. Methods Enzymol. 343:2002;170-182.
29. Lakovicz, J.R., 1999. Principles of Fluorescence Spectroscopy. Kluwer Academic/Plenum Publishers, New York, NY.
30. Li M., Lester H.A. Early fluorescence signals detect transitions at mammalian serotonin transporters. Biophys. J. 83:2002;206-218.
31. Li M., Farley R.A., Lester H.A. An intermediate state of the gamma-aminobutyric acid transporter GAT1 revealed by simultaneous voltage clamp and fluorescence. J. Gen. Physiol. 115:2000;491-508.
32. Lin Z., Uhl G.R. Dopamine transporter mutants with cocaine resistance and normal dopamine uptake provide targets for cocaine antagonism. Mol. Pharmacol. 61:2002;885-891.
33. Lin Z., Itokawa M., Uhl G.R. Dopamine transporter proline mutations influence dopamine uptake, cocaine analog recognition, and expression. FASEB J. 14:2000;715-728.
34. Lin Z., Wang W., Uhl G.R. Dopamine transporter tryptophan mutants highlight candidate dopamine- and cocaine-selective domains. Mol. Pharmacol. 58:2000;1581-1592.
35. Loland C.J., Norregaard L., Gether U. Defining proximity relationships in the tertiary structure of the dopamine transporter. Identification of a conserved glutamic acid as a third coordinate in the endogenous Zn(2+)-binding site. J. Biol. Chem. 274:1999;36928-36934.
36. Loland C.J., Norregaard L., Litman T., Gether U. Generation of an activating Zn(2+) switch in the dopamine transporter: mutation of an intracellular tyrosine constitutively alters the conformational equilibrium of the transport cycle. Proc. Natl. Acad. Sci. 99:2002;1683-1688.
37. Magde D., Elson E.L., Webb W.W. Thermodynamic fluctuations in a reacting system - measurement by fluorescence correlation spectroscopy. Phys. Rev. Lett. 29:1972;705-708.
38. Mannuzzu L.M., Moronne M.M., Isacoff E.Y. Direct physical measure of conformational rearrangement underlying potassium channel gating. Science. 271:1996;213-216.
39. Meinild A.K., Hirayama B.A., Wright E.M., Loo D.D. Fluorescence studies of ligand-induced conformational changes of the Na(+)/glucose cotransporter. Biochemistry. 41:2002;1250-1258.
40. Norgaard-Nielsen K., Norregaard L., Hastrup H., Javitch J.A., Gether U. Zn(2+) site engineering at the oligomeric interface of the dopamine transporter. FEBS Lett. 524:2002;87-91.
41. Norregaard L., Gether U. The monoamine neurotransmitter transporters: structure, conformational changes and molecular gating. Curr. Opin. Drug Discov. Dev. 4:2001;591-601.
42. Norregaard L., Frederiksen D., Nielsen E.O., Gether U. Delineation of an endogenous zinc-binding site in the human dopamine transporter. EMBO J. 17:1998;4266-4273.
43. Norregaard L., Visiers I., Loland C.J., Ballesteros J., Weinstein H., Gether U. Structural probing of a microdomain in the dopamine transporter by engineering of artificial Zn(2+) binding sites. Biochemistry. 39:2000;15836-15846.
44. Norregaard L., Loland C.J., Gether U. Evidence for distinct sodium, dopamine and cocaine dependent conformational changes in transmembrane segments 7 and 8 of the dopamine transporter. J. Biol. Chem. 278:2003;30587-30596.
45. Patel R.C., Kumar U., Lamb D.C., Eid J.S., Rocheville M., Grant M., Rani A., Hazlett T., Patel S.C., Gratton E., Patel Y.C. Ligand binding to somatostatin receptors induces receptor-specific oligomer formation in live cells. Proc. Natl. Acad. Sci. 99:2002;3294-3299.
46. Pitschke M., Prior R., Haupt M., Riesner D. Detection of single amyloid beta-protein aggregates in the cerebrospinal fluid of Alzheimer's patients by fluorescence correlation spectroscopy. Nat. Med. 4:1998;832-834.
47. Povlock S.L., Amara S.G. The structure and function of norepinephrine, dopamine, and serotonin transporters. Reith M.E.A. Neurotransmitter Transporters: Structure, Function, and Regulation. 1997;1-28 Humana Press, Totowa, NJ.
48. Rasmussen S.G., Carroll F.I., Maresch M.J., Jensen A.D., Tate C.G., Gether U. Biophysical characterization of the cocaine binding pocket in the serotonin transporter using a fluorescent cocaine analogue as a molecular reporter. J. Biol. Chem. 276:2001;4717-4723.
49. Rigler R., Elson E.S. Fluorescence Correlation Spectroscopy: Theory and Applications. 2001;487 Springer, New York, NY.
50. Rigler R., Mets U., Widengren J., Kask P. Fluorescence correlation spectroscopy with high count rate and low background: analysis of translational diffusion. Eur. Biophys. J. 22:1993;169-175.
51. Rigler R., Pramanik A., Jonasson P., Kratz G., Jansson O.T., Nygren P., Stahl S., Ekberg K., Johansson B., Uhlen S., Uhlen M., Jornvall H., Wahren J. Specific binding of proinsulin C-peptide to human cell membranes. Proc. Natl. Acad. Sci. 96:1999;13318-13323.
52. Rudnick G. Mechanisms of biogenic amine neurotransporters. Reith M.E.A. Neurotransmitter Transporters: Structure, Function, and Regulation. 1997;73-100 Humana Press, Totowa, NJ.
53. Schmid J.A., Scholze P., Kudlacek O., Freissmuth M., Singer E.A., Sitte H.H. Oligomerization of the human serotonin transporter and of the rat GABA transporter 1 visualized by fluorescence resonance energy transfer microscopy in living cells. J. Biol. Chem. 8:2000;8.
54. Schmid J.A., Just H., Sitte H.H. Impact of oligomerization on the function of the human serotonin transporter. Biochem. Soc. Trans. 29:2001;732-736.
55. Schwartz J.W., Blakely R.D., DeFelice L.J. Binding and transport in norepinephrine transporters. Real-time, spatially resolved analysis in single cells using a fluorescent substrate. J. Biol. Chem. 278:2003;9768-9777.
56. Torres G.E., Gainetdinov R.R., Caron M.G. Plasma membrane monoamine transporters: structure, regulation and function. Nat. Rev. Neurosci. 4:2003;13-25.
57. Tota R.T., Strader C.D. Characterization of the binding domain of the beta-adrenergic receptor with the fluorescent antagonist carazolol. J. Biol. Chem. 265:1990;16891-16897.
58. Turcatti G., Zoffmann S., Lowe J.A.R., Drozda S.E., Chassaing G., Schwartz T.W., Chollet A. Characterization of non-peptide antagonist and peptide agonist binding sites of the NK1 receptor with fluorescent ligands. J. Biol. Chem. 272:1997;21167-21175.
59. Van Craenenbroeck E., Engelborghs Y. Quantitative characterization of the binding of fluorescently labeled colchicine to tubulin in vitro using fluorescence correlation spectroscopy. Biochemistry. 38:1999;5082-5088.
60. Vaughan R.A., Agoston G.E., Lever J.R., Newman A.H. Differential binding of tropane-based photoaffinity ligands on the dopamine transporter. J. Neurosci. 19:1999;630-636.
61. Vaughan R.A., Gaffaney J.D., Lever J.R., Reith M.E., Dutta A.K. Dual incorporation of photoaffinity ligands on dopamine transporters implicates proximity of labeled domains. Mol. Pharmacol. 59:2001;1157-1164.
62. Wohland T., Friedrich K., Hovius R., Vogel H. Study of ligand-receptor interactions by fluorescence correlation spectroscopy with different fluorophores: evidence that the homopentameric 5-hydroxytryptamine type 3As receptor binds only one ligand. Biochemistry. 38:1999;8671-8681.
63. Wu X., Gu H.H. Cocaine affinity decreased by mutations of aromatic residue phenylalanine 105 in the transmembrane domain 2 of dopamine transporter. Mol. Pharmacol. 63:2003;653-658.
64. Zoffmann S., Chollet A., Galzi J.L. Identification of the extracellular loop 2 as the point of interaction between the N terminus of the chemokine MIP-1alpha and its CCR1 receptor. Mol. Pharmacol. 62:2002;729-736.
65. Zou M.F., Kopajtic T., Katz J.L., Wirtz S., Justice J.B. Jr., Newman A.H. Novel tropane-based irreversible ligands for the dopamine transporter. J. Med. Chem. 44:2001;4453-4461.