Electrical coupling between the human serotonin transporter and voltage-gated Ca2+ channels

Cell Calcium

Volumn 56, Issue 1, 2014, Pages 25-33

  Ruchala, Iwona ^a   Cabra, Vanessa ^a   Solis, Ernesto ^a   Glennon, Richard A ^a   De Felice, Louis J ^a   Eltit, Jose M ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Calcium channels; Calcium imaging; Excitability; L type calcium channel; Monoamine transporters; N type calcium channel; Neurotransmitter transport; Skeletal muscle

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL N TYPE; SEROTONIN TRANSPORTER; VOLTAGE GATED CALCIUM CHANNEL; CALCIUM CHANNEL; NEUROMUSCULAR DEPOLARIZING AGENT; SEROTONIN; CALCIUM CHANNEL CAV1.3; CALCIUM CHANNEL CAV2.2; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOPAMINE RELEASE; EXCITATION CONTRACTION COUPLING; HUMAN; HUMAN CELL; MEMBRANE DEPOLARIZATION; MOUSE; MUSCLE CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEROTONIN RELEASE; ANIMAL; CALCIUM SIGNALING; CELL MEMBRANE PERMEABILITY; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; METABOLISM; MYOBLAST; PHYSIOLOGY; SKELETAL MUSCLE; TRANSGENE; CALCIUM CURRENT; CALCIUM TRANSPORT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL MEMBRANE PERMEABILITY; EXCITATION CONTRACTION COUPLING; HEK293 CELLS; HUMANS; MICE; MUSCLE, SKELETAL; MYOBLASTS; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; NEUROMUSCULAR DEPOLARIZING AGENTS; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; TRANSGENES;

EID: 84901975604     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.04.003     Document Type: Article

References (48)

1. Kristensen A.S., Andersen J., Jorgensen T.N., Sorensen L., Eriksen J., Loland C.J., Stromgaard K., Gether U. SLC6 neurotransmitter transporters: structure, function, and regulation. Pharmacol. Rev. 2011, 63:585-640.
2. Torres G.E., Gainetdinov R.R., Caron M.G. Plasma membrane monoamine transporters: structure, regulation and function. Nat. Rev. Neurosci. 2003, 4:13-25.
3. Wilens T.E., Morrison N.R., Prince J. An update on the pharmacotherapy of attention-deficit/hyperactivity disorder in adults. Expert Rev. Neurother. 2011, 11:1443-1465.
4. Mandrioli R., Mercolini L., Saracino M.A., Raggi M.A. Selective serotonin reuptake inhibitors (SSRIs): therapeutic drug monitoring and pharmacological interactions. Curr. Med. Chem. 2012, 19:1846-1863.
5. Howell L.L., Kimmel H.L. Monoamine transporters and psychostimulant addiction. Biochem. Pharmacol. 2008, 75:196-217.
6. Steele T.D., McCann U.D., Ricaurte G.A. 3,4-Methylenedioxymethamphetamine (MDMA, Ecstasy): pharmacology and toxicology in animals and humans. Addiction 1994, 89:539-551.
7. Bedi G., Hyman D., de Wit H. Is ecstasy an empathogen? Effects of +/-3,4-methylenedioxymethamphetamine on prosocial feelings and identification of emotional states in others. Biol. Psychiatry 2010, 68:1134-1140.
8. Scahill L., Anderson G.M. Is ecstasy an empathogen?. Biol. Psychiatry 2010, 68:1082-1083.
9. Sulzer D., Sonders M.S., Poulsen N.W., Galli A. Mechanisms of neurotransmitter release by amphetamines: a review. Prog. Neurobiol. 2005, 75:406-433.
10. Fleckenstein A.E., Volz T.J., Riddle E.L., Gibb J.W., Hanson G.R. New insights into the mechanism of action of amphetamines. Annu. Rev. Pharmacol. Toxicol. 2007, 47:681-698.
11. Ingram S.L., Prasad B.M., Amara S.G. Dopamine transporter-mediated conductances increase excitability of midbrain dopamine neurons. Nat. Neurosci. 2002, 5:971-978.
12. Catterall W.A. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 2011, 3:a003947.
13. Colgan L.A., Cavolo S.L., Commons K.G., Levitan E.S. Action potential-independent and pharmacologically unique vesicular serotonin release from dendrites. J. Neurosci. 2012, 32:15737-15746.
14. Putzier I., Kullmann P.H., Horn J.P., Levitan E.S. Cav1.3 channel voltage dependence, not Ca2+ selectivity, drives pacemaker activity and amplifies bursts in nigral dopamine neurons. J. Neurosci. 2009, 29:15414-15419.
15. Garcia J., Beam K.G. Measurement of calcium transients and slow calcium current in myotubes. J. Gen. Physiol. 1994, 103:107-123.
16. Powell J.A., Petherbridge L., Flucher B.E. Formation of triads without the dihydropyridine receptor alpha subunits in cell lines from dysgenic skeletal muscle. J. Cell Biol. 1996, 134:375-387.
17. Helton T.D., Xu W., Lipscombe D. Neuronal L-type calcium channels open quickly and are inhibited slowly. J. Neurosci. 2005, 25:10247-10251.
18. Mager S., Min C., Henry D.J., Chavkin C., Hoffman B.J., Davidson N., Lester H.A. Conducting states of a mammalian serotonin transporter. Neuron 1994, 12:845-859.
19. Sonders M.S., Amara S.G. Channels in transporters. Curr. Opin. Neurobiol. 1996, 6:294-302.
20. Carvelli L., McDonald P.W., Blakely R.D., Defelice L.J. Dopamine transporters depolarize neurons by a channel mechanism. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16046-16051.
21. Lin F., Lester H.A., Mager S. Single-channel currents produced by the serotonin transporter and analysis of a mutation affecting ion permeation. Biophys. J. 1996, 71:3126-3135.
22. DeFelice L.J., Goswami T. Transporters as channels. Annu. Rev. Physiol. 2007, 69:87-112.
23. Sonders M.S., Zhu S.J., Zahniser N.R., Kavanaugh M.P., Amara S.G. Multiple ionic conductances of the human dopamine transporter: the actions of dopamine and psychostimulants. J. Neurosci. 1997, 17:960-974.
24. Galli A., Blakely R.D., DeFelice L.J. Norepinephrine transporters have channel modes of conduction. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:8671-8676.
25. Takekura H., Bennett L., Tanabe T., Beam K.G., Franzini-Armstrong C. Restoration of junctional tetrads in dysgenic myotubes by dihydropyridine receptor cDNA. Biophys. J. 1994, 67:793-803.
26. Paolini C., Protasi F., Franzini-Armstrong C. The relative position of RyR feet and DHPR tetrads in skeletal muscle. J. Mol. Biol. 2004, 342:145-153.
27. Tanabe T., Beam K.G., Adams B.A., Niidome T., Numa S. Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature 1990, 346:567-569.
28. Bidaud I., Monteil A., Nargeot J., Lory P. Properties and role of voltage-dependent calcium channels during mouse skeletal muscle differentiation. J. Muscle Res. Cell Motil. 2006, 27:75-81.
29. Eltit J.M., Szpyt J., Li H., Allen P.D., Perez C.F. Reduced gain of excitation-contraction coupling in triadin-null myotubes is mediated by the disruption of FKBP12/RyR1 interaction. Cell Calcium 2011, 49:128-135.
30. Eltit J.M., Bannister R.A., Moua O., Altamirano F., Hopkins P.M., Pessah I.N., Molinski T.F., Lopez J.R., Beam K.G., Allen P.D. Malignant hyperthermia susceptibility arising from altered resting coupling between the skeletal muscle L-type Ca2+ channel and the type 1 ryanodine receptor. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7923-7928.
31. Eltit J.M., Yang T., Li H., Molinski T.F., Pessah I.N., Allen P.D., Lopez J.R. RyR1-mediated Ca2+ leak and Ca2+ entry determine resting intracellular Ca2+ in skeletal myotubes. J. Biol. Chem. 2010, 285:13781-13787.
32. Johnson S.W., North R.A. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J. Physiol. 1992, 450:455-468.
33. Beckstead M.J., Grandy D.K., Wickman K., Williams J.T. Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 2004, 42:939-946.
34. Washburn C.P., Sirois J.E., Talley E.M., Guyenet P.G., Bayliss D.A. Serotonergic raphe neurons express TASK channel transcripts and a TASK-like pH- and halothane-sensitive K+ conductance. J. Neurosci. 2002, 22:1256-1265.
35. Deignan J., Lujan R., Bond C., Riegel A., Watanabe M., Williams J.T., Maylie J., Adelman J.P. SK2 and SK3 expression differentially affect firing frequency and precision in dopamine neurons. Neuroscience 2012, 217:67-76.
36. Branch S.Y., Beckstead M.J. Methamphetamine produces bidirectional, concentration-dependent effects on dopamine neuron excitability and dopamine-mediated synaptic currents. J. Neurophysiol. 2012, 108:802-809.
37. Vaarmann A., Gandhi S., Gourine A.V., Abramov A.Y. Novel pathway for an old neurotransmitter: dopamine-induced neuronal calcium signalling via receptor-independent mechanisms. Cell Calcium 2010, 48:176-182.
38. Lau T., Horschitz S., Berger S., Bartsch D., Schloss P. Antidepressant-induced internalization of the serotonin transporter in serotonergic neurons. FASEB J. 2008, 22:1702-1714.
39. Sukiasyan N., Hultborn H., Zhang M. Distribution of calcium channel Ca(V)1.3 immunoreactivity in the rat spinal cord and brain stem. Neuroscience 2009, 159:217-235.
40. Busquet P., Nguyen N.K., Schmid E., Tanimoto N., Seeliger M.W., Ben-Yosef T., Mizuno F., Akopian A., Striessnig J., Singewald N. CaV1.3 L-type Ca2+ channels modulate depression-like behaviour in mice independent of deaf phenotype. Int. J. Neuropsychopharmacol. 2010, 13:499-513.
41. Casamassima F., Hay A.C., Benedetti A., Lattanzi L., Cassano G.B., Perlis R.H. L-type calcium channels and psychiatric disorders: a brief review. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 2010, 153B:1373-1390.
42. Chan C.S., Guzman J.N., Ilijic E., Mercer J.N., Rick C., Tkatch T., Meredith G.E., Surmeier D.J. 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 2007, 447:1081-1086.
43. Lipscombe D., Helton T.D., Xu W. L-type calcium channels: the low down. J. Neurophysiol. 2004, 92:2633-2641.
44. Li H., Ding X., Lopez J.R., Takeshima H., Ma J., Allen P.D., Eltit J.M. Impaired Orai1-mediated resting Ca2+ entry reduces the cytosolic [Ca2+] and sarcoplasmic reticulum Ca2+ loading in quiescent junctophilin 1 knock-out myotubes. J. Biol. Chem. 2010, 285:39171-39179.
45. Eltit J.M., Li H., Ward C.W., Molinski T., Pessah I.N., Allen P.D., Lopez J.R. Orthograde dihydropyridine receptor signal regulates ryanodine receptor passive leak. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7046-7051.
46. Fahlke C., Zachar E., Rudel R. Single-channel recordings of chloride currents in cultured human skeletal muscle. Pflugers Arch. 1992, 421:108-116.
47. Dulhunty A.F. Distribution of potassium and chloride permeability over the surface and T-tubule membranes of mammalian skeletal muscle. J. Membr. Biol. 1979, 45:293-310.
48. Solis E., Zdravkovic I., Tomlinson I.D., Noskov S.Y., Rosenthal S.J., De Felice L.J. 4-(4-(dimethylamino)phenyl)-1-methylpyridinium (APP+) is a fluorescent substrate for the human serotonin transporter. J. Biol. Chem. 2012, 287:8852-8863.