Ionic currents in the human serotonin transporter reveal inconsistencies in the alternating access hypothesis

Biophysical Journal

Volumn 85, Issue 3, 2003, Pages 1548-1559

  Adams, Scott V ^a   DeFelice, Louis J ^b  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE ION; ION CHANNEL; POTASSIUM ION; SEROTONIN; SEROTONIN TRANSPORTER; SODIUM ION;

ANIMAL CELL; ARTICLE; FROG; HUMAN; ION CURRENT; NONHUMAN; OOCYTE; STEADY STATE; VOLTAGE CLAMP;

ANIMALIA; ANURA;

EID: 0041821557     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74587-1     Document Type: Article

References (56)

1. Adams, S. V., and L. J. DeFelice. 2002. Flux coupling in the human serotonin transporter. Biophys. J. 83:3268-3282.
2. Blakely, R. D., L. J. DeFelice, and H. C. Hartzell. 1994. Molecular physiology of norepinephrine and serotonin transporters. J. Exp. Biol. 196:263-281.
3. Bunin, M. A., and R. M. Wightman. 1998. Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J. Neurosci. 18:4854-4860.
4. Cao, Y., M. Li, S. Mager, and H. A. Lester. 1998. Amino acid residues that control pH modulation of transport-associated current in mammalian serotonin transporters. J. Neurosci. 18:7739-7749.
5. + permeation and pH regulation at a mammalian serotonin transporter. J. Neurosci. 17:2257-2266.
6. Chen, X. Z., M. J. Coady, F. Jackson, A. Berteloot, and J. Y. Lapointe. 1995. Thermodynamic determination of the Na+: glucose coupling ratio for the human SGLT1 cotransporter. Biophys. J. 69:2405-2414.
7. Chen, X. Z., M. J. Coady, and J. Y. Lapointe. 1996. Fast voltage clamp discloses a new component of presteady-state currents from the Na(+)-glucose cotransporter. Biophys. J. 71:2544-2552.
8. Chen, J. J., Z. Li, H. Pan, D. L. Murphy, H. Tamir, H. Koepsell, and M. D. Gershon. 2001. Maintenance of serotonin in the intestinal mucosa and ganglia of mice that lack the serotonin transporter: abnormal intestinal motility and the expression of cation transporters. J. Neurosci. 21:6348-6361.
9. Chou, T. 1999. Kinetics and thermodynamics across single-file pores: solute permeability and rectified osmosis. J. Chem. Phys. 110:606-615.
10. Chou, T., and D. Lohse. 1999. Entropy-driven pumping in zeolites and biological membranes. Phys. Rev. Lett. 82:3552-3555.
11. Coady, M. J., X. Z. Chen, and J. Y. Lapointe. 1996. rBAT is an amino acid exchanger with variable stoichiometry. J. Membr. Biol. 149:1-8.
12. Coady, M. J., F. Jalal, X. Chen, G. Lemay, A. Berteloot, and J. Y. Lapointe. 1994. Electrogenic amino acid exchange via the rBAT transporter. FEBS Lett. 356:174-178.
13. Costa, A. C., J. W. Patrick, and J. A. Dani. 1994. Improved technique for studying ion channels expressed in Xenopus oocytes, including fast superfusion. Biophys. J. 67:395-401.
14. Dascal, N. 1987. The use of Xenopous oocytes for the study of ion channels. CRC. Crit. Rev. Biochem. 22:317-387.
15. DeFelice, L. J., and S. V. Adams. 2001. Serotonin and norepinephrine transporters: possible relationship between oligomeric structure and channel modes of conduction. Molecl. Memb. Biology. 18:45-51.
16. DeFelice, L. J., S. V. Adams, and D. Ypey, 2001, Single-file diffusion and neurotransmitter transporters: Hodgkin's mechanical model revisited. Biosystems. 62:57-66.
17. Eddahibi, S., M. Humbert, E. Fadel, B. Raffestin, M. Darmon, F. Capron, G. Simmmoneau, P. Dartevelle, M. Hamon, and S. Adnot. 2001. Serotonin transporter overexpression is responsible for pulmonary artery smooth muscle hyperplasia in primary pulmonary hypertension. J. Clin. Invest. 108:1141-1150.
18. Elsner, H.-A., H.-H. Honck, F. Willmann, H.-J. Kreienkamp, and F. Iglauer. 2000. Poor quality of oocytes from Xenopus laevis used in laboratory experiments: prevention by use of antiseptic surgical technique and antibiotic supplementation. Comp. Med. 50:206-211.
19. Galli, A., R. D. Blakely, and L. J. DeFelice. 1996. Norepinephrine transporters have channel modes of conduction. Proc. Natl. Acad. Sci. USA. 93:8671-8676.
20. Galli, A., R. D. Blakely, and L. J. DeFelice. 1998. Patch-clamp and amperometric recordings from norepinephrine transporters: channel activity and voltage-dependent uptake. Proc. Natl. Acad. Sci. USA. 95:13260-13265.
21. Galli, A., C. I. Petersen, M. deBlaquiere, R. D. Blakely, and L. J. DeFelice. 1997. Drosophila serotonin transporters have voltage-dependent uptake coupled to a serotonin-gated ion channel. J. Neurosci. 17:3401-3411.
22. Goldin, A. L. 1992. Maintenance of Xenopus laevis and oocyte injection. Methods Enzymol. 207:266-279.
23. Gu, H., S. C. Wall, and G. Rudnick. 1994. Stable expression of biogenic amine transporters reveals differences in inhibitor sensitivity, kinetics, and ion dependence. J. Biol. Chem. 269:7124-7130.
24. Gu, H., S. C. Wall, and G. Rudnick. 1996. Ion coupling stoichiometry for the norepinephrine transporter in membrane vesicles from stably transfected cells. J. Biol. Chem. 271:6911-6916.
25. Hilgemann, D. W., and C. C. Lu. 1999. GAT1 (GABA:Na+: Cl-) cotransport function. Database reconstruction with an alternating access model. J. Gen. Physiol. 114:459-475.
26. Hodgkin, A. L., and R. D. Keynes. 1955. The potassium permeability of a giant nerve fibre. J. Physiol. 128:61-88.
27. Ingram, S. L., and S. G. Amara. 2000. Arachidonic acid stimulates a novel cocaine-sensitive cation conductance associated with the human dopamine transporter. J. Neurosci. 20:550-557.
28. Iversen, L. L. 1971. Role of transmitter uptake mechanisms in synaptic neurotransmission. Br. J. Pharmacol. 41:571-591.
29. Jardetsky, O. 1966. Simple allosteric model for membrane pumps. Nature. 211:969-970.
30. Kaneko, S., A. Akaike, and M. Satoh. 1998. Cut-open recording techniques. Methods Enzymol. 293:319-331.
31. Keyes, S. R., and G. Rudnick. 1982. Coupling of transmembrane proton gradients to platelet serotonin transport. J. Biol. Chem. 257:1172-1176.
32. Kuruma, A., and H. C. Hartzell. 1999. Dynamics of calcium regulation of chloride currents in Xenopus oocytes. Am. J. Physiol. 276:C161-C175.
33. Läuger, P. 1991. Electrogenic Ion Pumps. Sinauer Associates, Sunderland, MA.
34. Li, M., R. A. Farley, and H. A. Lester. 2002. Voltage-dependent transient currents of human and rat 5-HT transporters (SERT) are blocked by HEPES and ion channel ligands. FEBS Lett. 513:247-252.
35. Lin, F., H. A. Lester, and S. Mager. 1996. Single-channel currents produced by the serotonin transporter and analysis of a mutation affecting ion permeation. Biophys. J. 71:3126-3135.
36. Loo, D. D. F., S. Eskandari, K. J. Boorer, H. K. Sarkar, and E. M. Wright. 2000. Role of Cl- in electrogenic Na+-coupled cotransporters GAT1 and SGLT1. J. Biol. Chem. 275:37414-37422.
37. Lu, C.-C., and D. Hilgemann. 1999. GAT1 (GABA:Na: Cl) cotransport function. J. Gen. Physiol. 114:429-444.
38. Mager, S., C. Min, D. J. Henry, C. Chavkin, B. J. Hoffman, N. Davidson, and H. A. Lester. 1994. Conducting states of a mammalian serotonin transporter. Neuron. 12:845-859.
39. Mager, S., J. Naeve, M. Quick, C. Labarca, N. Davidson, and H. A. Lester. 1993. Steady states, charge movements, and rates for a cloned GABA transporter expressed in Xenopus oocytes. Neuron. 10:177-188.
40. Nelson, P. J., and G. Rudnick. 1979. Coupling between platelet 5-hydroxytryptamine and potassium transport. J. Biol. Chem. 254:10084-10089.
41. Ni, Y. G., J. G. Chen, A. Androutsellis-Theotokis, C. J. Huang, E. Moczydlowski, and G. Rudnick. 2001. A lithium-induced conformational change in serotonin transporter alters cocaine binding, ion conductance, and reactivity of Cys-109. J. Biol. Chem. 276:30942-30947.
42. Petersen, C. I., and L. J. DeFelice. 1999. Ionic interactions in the Drosophila serotonin transporter identify it as a serotonin channel. Nat. Neurosci. 2:605-610.
43. Quick, M. W., J. Naeve, N. Davidson, and H. A. Lester. 1992. Incubation with horse serum increases viability and decreases background neurotransmitter uptake in Xenopus oocytes. Biotechniques. 13:357-361.
44. Ramamoorthy, S., A. L. Bauman, K. R. Moore, H. Han, T. Yang-Feng, A. S. Chang, V. Ganapathy, and R. D. Blakely. 1993. Antidepressant- and cocaine-sensitive human serotonin transporter: molecular cloning, expression, and chromosomal localization. Proc. Natl. Acad. Sci. USA. 90:2542-2546.
45. Ramsey, I. S., and L. J. DeFelice. 2002. Serotonin transporter function and pharmacology are sensitive to expression level: evidence for an endogenous regulatory factor. J. Biol. Chem. 277:14475-14482.
46. Rudnick, G. 1977. Active transport of 5-hydroxytryptamine by plasma membrane vesicles isolated from human blood platelets. J. Biol. Chem. 252:2170-2174.
47. Rudnick, G. 1998. Ion-coupled neurotransmitter transport: thermodynamic vs. kinetic determinations of stoichiometry. Methods Enzymol. 296:233-247.
48. Rudnick, G., and J. Clark. 1993. From synapse to vesicle: the reuptake and storage of biogenic amine neurotransmitters. Biochim. Biophys. Acta. 1144:249-263.
49. Rudnick, G., and P. J. Nelson. 1978. Platelet 5-hydroxytryptamine transport, an electroneutral mechanism coupled to potassium. Biochem. 17:4739-4742.
50. Sitte, H. H., B. Hiptmair, J. Zwach, C. Pifl, E. A. Singer, and P. Scholze. 2001. Quantitative analysis of inward and outward transport rate in cells stably expressing the cloned human serotonin transporter: inconsistencies with the hypothesis of facilitated transport. Molecl. Pharmacol. 59:1129-1137.
51. Sitte, H. H., P. Scholze, P. Schloss, C. Pifl, and E. A. Singer. 2000. Characterization of carrier-mediated efflux in human embryonic kidney 293 cells stably expressing the rat serotonin transporter: a superfusion study. J. Neurochem. 74:1317-1324.
52. Sonders, M. S., and S. G. Amara. 1996. Channels in transporters. Curr. Opin. Neurobiol. 6:294-302.
53. Sonders, M. S., S. J. Zhu, N. R. Zahniser, M. P. Kavanaugh, and S. G. Amara. 1997. Multiple ionic conductances of the human dopamine transporter: the actions of dopamine and psychostimulants. J. Neurosci. 17:960-974.
54. Stefani, E., and F. Bezanilla. 1998. Cut-open oocyte voltage-clamp technique. Methods Enzymol. 293:300-318.
55. Stein, W. D. 1986. Transport and Diffusion Across Cell Membranes. Academic Press, New York.
56. Stuhmer, W. 1998. Electrophysiologic recordings from Xenopus oocytes. Methods Enzymol. 293:280-300.