Calmodulin Kinase II Interacts with the Dopamine Transporter C Terminus to Regulate Amphetamine-Induced Reverse Transport

Neuron

Volumn 51, Issue 4, 2006, Pages 417-429

  Fog, Jacob U ^a,b   Khoshbouei, Habibeh ^c   Holy, Marion ^d   Owens, William A ^e   Vaegter, Christian Bjerggaard ^a   Sen, Namita ^f   Nikandrova, Yelyzaveta ^c   Bowton, Erica ^c   McMahon, Douglas G ^c   Colbran, Roger J ^c   Daws, Lynette C ^e   Sitte, Harald H ^d   Javitch, Jonathan A ^f   Galli, Aurelio ^c   Gether, Ulrik ^a  

^a Department of Pharmacology   (Denmark)

^b H LUNDBECK A S   (Denmark)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^f Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

CELLBIO; SIGNALING

Indexed keywords

AMPHETAMINE; DOPAMINE TRANSPORTER; PROTEIN KINASE (CALCIUM,CALMODULIN) II; SERINE;

AMINO TERMINAL SEQUENCE; AMPEROMETRY; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MUTATION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RAT; TRANSPORT KINETICS;

AMPHETAMINES; ANIMALS; ANIMALS, NEWBORN; BENZYLAMINES; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM STIMULANTS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; ENZYME INHIBITORS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MEMBRANE POTENTIALS; MESENCEPHALON; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; SULFONAMIDES; TRANSFECTION;

EID: 33747141753     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.06.028     Document Type: Article

References (42)

1. Amara S.G., and Kuhar M.J. Neurotransmitter transporters: recent progress. Annu. Rev. Neurosci. 16 (1993) 73-93
2. Bjerggaard C., Fog J., Hastrup H., Madsen K., Javitch J.A., and Gether U. Surface targeting of the dopamine transporter involves discrete epitopes in the distal carboxyterminus but occurs independently of canonical PDZ domain interactions. J. Neurosci. 24 (2004) 7024-7036
3. Callaghan P.D., Irvine R.J., and Daws L.C. Differences in the in vivo dynamics of neurotransmitter release and serotonin uptake after acute para-methoxyamphetamine and 3,4-methylenedioxymethamphetamine revealed by chronoamperometry. Neurochem. Int. 47 (2005) 350-361
4. Cervinski M.A., Foster J.D., and Vaughan R.A. Psychoactive substrates stimulate dopamine transporter phosphorylation and down regulation by cocaine sensitive and protein kinase C dependent mechanisms. J. Biol. Chem. 280 (2005) 40442-40449
5. Chen N.H., Reith M.E., and Quick M.W. Synaptic uptake and beyond: the sodium- and chloride-dependent neurotransmitter transporter family SLC6. Pflugers Arch. 447 (2004) 519-531
6. Colbran R.J. Targeting of calcium/calmodulin-dependent protein kinase II. Biochem. J. 378 (2003) 1-16
7. Daws L.C., Irvine R.J., Callaghan P.D., Toop N.P., White J.M., and Bochner F. Differential behavioural and neurochemical effects of para-methoxyamphetamine and 3,4-methylenedioxymethamphetamine in the rat. Prog. Neuropsychopharmacol. Biol. Psychiatry 24 (2000) 955-977
8. Falkenburger B.H., Barstow K.L., and Mintz I.M. Dendrodendritic inhibition through reversal of dopamine transport. Science 293 (2001) 2465-2470
9. Fischer J.F., and Cho A.K. Chemical release of dopamine from striatal homogenates: evidence for an exchange diffusion model. J. Pharmacol. Exp. Ther. 208 (1979) 203-209
10. Galli A., Petersen C.I., deBlaquiere M., Blakely R.D., and DeFelice L.J. Drosophila serotonin transporters have voltage-dependent uptake coupled to a serotonin-gated ion channel. J. Neurosci. 17 (1997) 3401-3411
11. Gardoni F., Schrama L.H., van Dalen J.J., Gispen W.H., Cattabeni F., and Di Luca M. AlphaCaMKII binding to the C-terminal tail of NMDA receptor subunit NR2A and its modulation by autophosphorylation. FEBS Lett. 456 (1999) 394-398
12. Gnegy M.E. The effect of phosphorylation on amphetamine-mediated outward transport. Eur. J. Pharmacol. 479 (2003) 83-91
13. Gnegy M.E., Khoshbouei H., Berg K.A., Javitch J.A., Clarke W.P., Zhang M., and Galli A. Intracellular Ca2+ regulates amphetamine-induced dopamine efflux and currents mediated by the human dopamine transporter. Mol. Pharmacol. 66 (2004) 137-143
14. Granas C., Ferrer J., Loland C.J., Javitch J.A., and Gether U. N-terminal truncation of the dopamine transporter abolishes phorbol ester- and substance P receptor-stimulated phosphorylation without impairing transporter internalization. J. Biol. Chem. 278 (2003) 4990-5000
15. Griffith L.C. Regulation of calcium/calmodulin-dependent protein kinase II activation by intramolecular and intermolecular interactions. J. Neurosci. 24 (2004) 8394-8398
16. Iwata S.I., Hewlett G.H., Ferrell S.T., Kantor L., and Gnegy M.E. Enhanced dopamine release and phosphorylation of synapsin I and neuromodulin in striatal synaptosomes after repeated amphetamine. J. Pharmacol. Exp. Ther. 283 (1997) 1445-1452
17. Jardetzky O. Simple allosteric model for membrane pumps. Nature 211 (1966) 969-970
18. Johnson L.A., Guptaroy B., Lund D., Shamban S., and Gnegy M.E. Regulation of amphetamine-stimulated dopamine efflux by protein kinase C beta. J. Biol. Chem. 280 (2005) 10914-10919
19. Kahlig K.M., Binda F., Khoshbouei H., Blakely R.D., McMahon D.G., Javitch J.A., and Galli A. Amphetamine induces dopamine efflux through a dopamine transporter channel. Proc. Natl. Acad. Sci. USA 102 (2005) 3495-3500
20. Kantor L., Hewlett G.H., and Gnegy M.E. Enhanced amphetamine- and K+-mediated dopamine release in rat striatum after repeated amphetamine: differential requirements for Ca2+- and calmodulin-dependent phosphorylation and synaptic vesicles. J. Neurosci. 19 (1999) 3801-3808
21. Khoshbouei H., Wang H., Lechleiter J.D., Javitch J.A., and Galli A. Amphetamine-induced dopamine efflux. A voltage-sensitive and intracellular Na+-dependent mechanism. J. Biol. Chem. 278 (2003) 12070-12077
22. Khoshbouei H., Sen N., Guptaroy B., Johnson L., Lund D., Gnegy M.E., Galli A., and Javitch J.A. N-terminal phosphorylation of the dopamine transporter is required for amphetamine-induced efflux. PLoS Biol. 2 (2004) E78
23. Lieberman J.A., Sheitman B.B., and Kinon B.J. Neurochemical sensitization in the pathophysiology of schizophrenia: deficits and dysfunction in neuronal regulation and plasticity. Neuropsychopharmacology 17 (1997) 205-229
24. Loland C.J., Norgaard-Nielsen K., and Gether U. Probing dopamine transporter structure and function by Zn2+-site engineering. Eur. J. Pharmacol. 479 (2003) 187-197
25. Loland C.J., Granas C., Javitch J.A., and Gether U. Identification of intracellular residues in the dopamine transporter critical for regulation of transporter conformation and cocaine binding. J. Biol. Chem. 279 (2004) 3228-3238
26. Montanez S., Owens W.A., Gould G.G., Murphy D.L., and Daws L.C. Exaggerated effect of fluvoxamine in heterozygote serotonin transporter knockout mice. J. Neurochem. 86 (2003) 210-219
27. Pierce R.C., and Kalivas P.W. Repeated cocaine modifies the mechanism by which amphetamine releases dopamine. J. Neurosci. 17 (1997) 3254-3261
28. Pifl C., and Singer E.A. Ion dependence of carrier-mediated release in dopamine or norepinephrine transporter-transfected cells questions the hypothesis of facilitated exchange diffusion. Mol. Pharmacol. 56 (1999) 1047-1054
29. Rawson R.A., Gonzales R., and Brethen P. Treatment of methamphetamine use disorders: an update. J. Subst. Abuse Treat. 23 (2002) 145-150
30. Rayport S., Sulzer D., Shi W.X., Sawasdikosol S., Monaco J., Batson D., and Rajendran G. Identified postnatal mesolimbic dopamine neurons in culture: morphology and electrophysiology. J. Neurosci. 12 (1992) 4264-4280
31. Robison A.J., Bass M.A., Jiao Y., MacMillan L.B., Carmody L.C., Bartlett R.K., and Colbran R.J. Multivalent interactions of calcium/calmodulin-dependent protein kinase II with the postsynaptic density proteins NR2B, densin-180, and alpha-actinin-2. J. Biol. Chem. 280 (2005) 35329-35336
32. Rose C.R. Na+ signals at central synapses. Neuroscientist 8 (2002) 532-539
33. Rose C.R., and Konnerth A. NMDA receptor-mediated Na+ signals in spines and dendrites. J. Neurosci. 21 (2001) 4207-4214
34. Saunders C., Ferrer J.V., Shi L., Chen J., Merrill G., Lamb M.E., Leeb-Lundberg L.M., Carvelli L., Javitch J.A., and Galli A. Amphetamine-induced loss of human dopamine transporter activity: an internalization-dependent and cocaine-sensitive mechanism. Proc. Natl. Acad. Sci. USA 97 (2000) 6850-6855
35. Scholze P., Norregaard L., Singer E.A., Freissmuth M., Gether U., and Sitte H.H. The role of zinc ions in reverse transport mediated by monoamine transporters. J. Biol. Chem. 276 (2002) 40476-40485
36. Sitte H.H., Huck S., Reither H., Boehm S., Singer E.A., and Pifl C. Carrier-mediated release, transport rates, and charge transfer induced by amphetamine, tyramine, and dopamine in mammalian cells transfected with the human dopamine transporter. J. Neurochem. 71 (1998) 1289-1297
37. Strack S., Robison A.J., Bass M.A., and Colbran R.J. Association of calcium/calmodulin-dependent kinase II with developmentally regulated splice variants of the postsynaptic density protein densin-180. J. Biol. Chem. 275 (2000) 25061-25064
38. Sulzer D., Sonders M.S., Poulsen N.W., and Galli A. Mechanisms of neurotransmitter release by amphetamines: A review. Prog. Neurobiol. 75 (2005) 406-433
39. Torres G.E., Yao W.D., Mohn A.R., Quan H., Kim K.M., Levey A.I., Staudinger J., and Caron M.G. Functional interaction between monoamine plasma membrane transporters and the synaptic PDZ domain-containing protein PICK1. Neuron 30 (2001) 121-134
40. Torres G.E., Gainetdinov R.R., and Caron M.G. Plasma membrane monoamine transporters: structure, regulation and function. Nat. Rev. Neurosci. 4 (2003) 13-25
41. Walikonis R.S., Oguni A., Khorosheva E.M., Jeng C.J., Asuncion F.J., and Kennedy M.B. Densin-180 forms a ternary complex with the (alpha)-subunit of Ca2+/calmodulin-dependent protein kinase II and (alpha)-actinin. J. Neurosci. 21 (2001) 423-433
42. Wall S.C., Gu H., and Rudnick G. Biogenic amine flux mediated by cloned transporters stably expressed in cultured cell lines: amphetamine specificity for inhibition and efflux. Mol. Pharmacol. 47 (1995) 544-550