Melittin initiates dopamine transporter internalization and recycling in transfected HEK-293 cells

European Journal of Pharmacology

Volumn 690, Issue 1-3, 2012, Pages 13-21

  Keith, Dove J ^a,c   Wolfrum, Katherine ^a   Eshleman, Amy J ^a,b   Janowsky, Aaron ^a,b  

^a PORTLAND VA MEDICAL CENTER   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

Dopamine transporter; Melittin; Protein kinase; Trafficking

Indexed keywords

CLATHRIN; COCAINE; DOPAMINE; DOPAMINE TRANSPORTER; EARLY ENDOSOME ANTIGEN 1; GUANINE NUCLEOTIDE BINDING PROTEIN; MELITTIN; RAB11 PROTEIN; RAB5A PROTEIN; RAB7 PROTEIN; RECOMBINANT DOPAMINE TRANSPORTER; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; ENDOSOME; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN TRANSPORT;

BIOTINYLATION; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; HEK293 CELLS; HUMANS; INTRACELLULAR SPACE; MELITTEN; PROTEIN TRANSPORT; TETRADECANOYLPHORBOL ACETATE; TRANSFECTION;

EID: 84864420564     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2012.05.020     Document Type: Article

References (48)

1. J. Adler, and I. Parmryd Quantifying colocalization by correlation: the Pearson correlation coefficient is superior to the Mander's overlap coefficient Cytometry A 77 2010 733 742
2. S.G. Amara, and M.J. Kuhar Neurotransmitter transporters: recent progress Annu. Rev. Neurosci. 16 1993 73 93
3. M.A. Cervinski, J.D. Foster, and R.A. Vaughan 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
4. M.Y. Chang, S.H. Lee, J.H. Kim, K.H. Lee, Y.S. Kim, H. Son, and Y.S. Lee Protein kinase C-mediated functional regulation of dopamine transporter is not achieved by direct phosphorylation of the dopamine transporter protein J. Neurochem. 77 2001 754 761
5. L. Chi, and M.E. Reith Substrate-induced trafficking of the dopamine transporter in heterologously expressing cells and in rat striatal synaptosomal preparations J. Pharmacol. Exp. Ther. 307 2003 729 736
6. D. Crippa, U. Schenk, M. Francolini, P. Rosa, C. Verderio, M. Zonta, T. Pozzan, M. Matteoli, and G. Carmignoto Synaptobrevin2-expressing vesicles in rat astrocytes: insights into molecular characterization, dynamics and exocytosis J. Physiol. 570 2006 567 582
7. G.M. Daniels, and S.G. Amara Regulated trafficking of the human dopamine transporter. Clathrin-mediated internalization and lysosomal degradation in response to phorbol esters J. Biol. Chem. 274 1999 35794 35801
8. S.L. Deken, D. Wang, and M.W. Quick Plasma membrane GABA transporters reside on distinct vesicles and undergo rapid regulated recycling J. Neurosci. 23 2003 1563 1568
9. J. Eriksen, W.E. Bjorn-Yoshimoto, T.N. Jorgensen, A.H. Newman, and U. Gether Postendocytic sorting of constitutively internalized dopamine transporter in cell lines and dopaminergic neurons J. Biol. Chem. 285 2010 27289 27301
10. J. Eriksen, S.G. Rasmussen, T.N. Rasmussen, C.B. Vaegter, J.H. Cha, M.F. Zou, A.H. Newman, and U. Gether Visualization of dopamine transporter trafficking in live neurons by use of fluorescent cocaine analogs J. Neurosci. 29 2009 6794 6808
11. A.J. Eshleman, M. Carmolli, M. Cumbay, C.R. Martens, K.A. Neve, and A. Janowsky Characteristics of drug interactions with recombinant biogenic amine transporters expressed in the same cell type J. Pharmacol. Exp. Ther. 289 1999 877 885
12. A.J. Eshleman, R.L. Neve, A. Janowsky, and K.A. Neve Characterization of a recombinant human dopamine transporter in multiple cell lines J. Pharmacol. Exp. Ther. 274 1995 276 283
13. J.D. Foster, S.D. Adkins, J.R. Lever, and R.A. Vaughan Phorbol ester induced trafficking-independent regulation and enhanced phosphorylation of the dopamine transporter associated with membrane rafts and cholesterol J. Neurochem. 105 2008 1683 1699
14. C.A. Furman, C.B. Lo, S. Stokes, J.A. Esteban, and M.E. Gnegy Rab 11 regulates constitutive dopamine transporter trafficking and function in N2A neuroblastoma cells Neurosci. Lett. 463 2009 78 81
15. C.E. Futter, A. Gibson, E.H. Allchin, S. Maxwell, L.J. Ruddock, G. Odorizzi, D. Domingo, I.S. Trowbridge, and C.R. Hopkins In polarized MDCK cells basolateral vesicles arise from clathrin-gamma-adaptin-coated domains on endosomal tubules J. Cell. Biol. 141 1998 611 623
16. M.S. Geddis, K. Tornieri, A. Giesecke, and V. Rehder PLA2 and secondary metabolites of arachidonic acid control filopodial behavior in neuronal growth cones Cell Motil. Cytoskeleton. 57 2004 53 67
17. J.E. Heuser, and R.G. Anderson Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation J. Cell Biol. 108 1989 389 400
18. L. Hunyady, A.J. Baukal, Z. Gaborik, J.A. Olivares-Reyes, M. Bor, M. Szaszak, R. Lodge, K.J. Catt, and T. Balla Differential PI 3-kinase dependence of early and late phases of recycling of the internalized AT1 angiotensin receptor J. Cell Biol. 157 2002 1211 1222
19. D.J. Keith, A.J. Eshleman, and A. Janowsky Melittin stimulates fatty acid release through non-phospholipase-mediated mechanisms and interacts with the dopamine transporter and other membrane-spanning proteins Eur. J. Pharmacol. 650 2011 501 510
20. S.Y. Lee, H.S. Park, S.J. Lee, and M.U. Choi Melittin exerts multiple effects on the release of free fatty acids from L1210 cells: lack of selective activation of phospholipase A2 by melittin Arch. Biochem. Biophys. 389 2001 57 67
21. M.K. Loder, and H.E. Melikian The dopamine transporter constitutively internalizes and recycles in a protein kinase C-regulated manner in stably transfected PC12 cell lines J. Biol. Chem. 278 2003 22168 22174
22. H.E. Melikian, and K.M. Buckley Membrane trafficking regulates the activity of the human dopamine transporter J. Neurosci. 19 1999 7699 7710
23. M. Miranda, C.C. Wu, T. Sorkina, D.R. Korstjens, and A. Sorkin Enhanced ubiquitylation and accelerated degradation of the dopamine transporter mediated by protein kinase C J. Biol. Chem. 280 2005 35617 35624
24. J.A. Moron, I. Zakharova, J.V. Ferrer, G.A. Merrill, B. Hope, E.M. Lafer, Z.C. Lin, J.B. Wang, J.A. Javitch, A. Galli, and T.S. Shippenberg Mitogen-activated protein kinase regulates dopamine transporter surface expression and dopamine transport capacity J. Neurosci. 23 2003 8480 8488
25. I.A. Muzzio, C.C. Gandhi, U. Manyam, A. Pesnell, and L.D. Matzel Receptor-stimulated phospholipase A(2) liberates arachidonic acid and regulates neuronal excitability through protein kinase C J. Neurophysiol. 85 2001 1639 1647
26. S. Nakamura Involvement of phospholipase A2 in axonal regneration of brain noradrenergic neurones Neuroreport 4 1993 371 374
27. K.A. Neve, R.A. Henningsen, J.R. Bunzow, and O. Civelli Functional characterization of a rat dopamine D-2 receptor cDNA expressed in a mammalian cell line Mol. Pharmacol. 36 1989 446 451
28. L. Palomba, M. Bianchi, T. Persichini, M. Magnani, M. Colasanti, and O. Cantoni Downregulation of nitric oxide formation by cytosolic phospholipase A2-released arachidonic acid Free Radical Biol. Med. 36 2004 319 329
29. L.H. Parsons, and J.B. Justice Jr. Quantitative approaches to in vivo brain microdialysis Crit. Rev. Neurobiol. 8 1994 189 220
30. S.R. Pfeffer Rab GTPases: specifying and deciphering organelle identity and function Trends Cell Biol. 11 2001 487 491
31. V.Y. Postupalenko, V.V. Schvadchak, G. Duportail, V.G. Pivovarenko, A.S. Klymchenko, and Y. Mely Monitoring membrane binding and insertion of peptides by two-color fluorescent label Biochim. Biophys. Acta. 1808 2011 424 432
32. Z.B. Pristupa, F. McConkey, F. Liu, H.Y. Man, F.J. Lee, Y.T. Wang, and H.B. Niznik Protein kinase-mediated bidirectional trafficking and functional regulation of the human dopamine transporter Synapse 30 1998 79 87
33. M.S. Reid, K. Hsu, B.K. Tolliver, C.A. Crawford, and S.P. Berger Evidence for the involvement of phospholipase A2 mechanisms in the development of stimulant sensitization J. Pharmacol. Exp. Ther. 276 1996 1244 1256
34. C. Saunders, J.V. Ferrer, L. Shi, J. Chen, G. Merrill, M.E. Lamb, L.M. Leeb-Lundberg, L. Carvelli, J.A. Javitch, and A. Galli Amphetamine-induced loss of human dopamine transporter activity: an internalization-dependent and cocaine-sensitive mechanism Proc. Nat. Acad. Sci. USA 97 2000 6850 6855
35. K.C. Schmitt, and M.E Reith Regulation of the dopamine transporter: aspects relevant to psychostimulant drugs of abuse Ann. N.Y. Acad. Sci. 1187 2010 316 340
36. D.R. Sheff, E.A. Daro, M. Hull, and I. Mellman The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions J. Cell Biol. 145 1999 123 139
37. B. Sonnichsen, S. De Renzis, E. Nielsen, J. Rietdorf, and M. Zerial Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11 J. Cell Biol. 149 2000 901 914
38. T. Sorkina, S. Doolen, E. Galperin, N.R. Zahniser, and A. Sorkin Oligomerization of dopamine transporters visualized in living cells by fluorescence resonance energy transfer microscopy J. Biol. Chem. 278 2003 28274 28283
39. T. Sorkina, B.R. Hoover, N.R. Zahniser, and A. Sorkin Constitutive and protein kinase C-induced internalization of the dopamine transporter is mediated by a clathrin-dependent mechanism Traffic 6 2005 157 170
40. E.N. Star, A.J. Newton, and V.N. Murthy Real-time imaging of Rab3a and Rab5a reveals differential roles in presynaptic function J. Physiol. 569 2005 103 117
41. W. Stoorvogel, V. Oorschot, and H.J. Geuze A novel class of clathrin-coated vesicles budding from endosomes J. Cell. Biol. 132 1996 21 33
42. I. Tommasini, P. Sestili, A. Guidarelli, and O. Cantoni Peroxynitrite stimulates the activity of cytosolic phospholipase A2 in U937 cells: the extent of arachidonic acid formation regulates the balance between cell survival or death Cell Death Differ. 9 2002 1368 1376
43. R.A. Vaughan, R.A. Huff, G.R. Uhl, and M.J. Kuhar Protein kinase C-mediated phosphorylation and functional regulation of dopamine transporters in striatal synaptosomes J. Biol. Chem. 272 1997 15541 15546
44. C. Wang, D.C. Buck, R. Yang, T.A. Macey, and K.A Neve Dopamine D2 receptor stimulation of mitogen-activated protein kinases mediated by cell type-dependent transactivation of receptor tyrosine kinases J. Neurochem. 93 2005 899 909
45. R.M. Wightman, and J.B. Zimmerman Control of dopamine extracellular concentration in rat striatum by impulse flow and uptake Brain Res. Brain Res. Rev. 15 1990 135 144
46. J.M. Wilson, M. de Hoop, N. Zorzi, B.H. Toh, C.G. Dotti, and R.G. Parton EEA1, a tethering protein of the early sorting endosome, shows a polarized distribution in hippocampal neurons, epithelial cells, and fibroblasts Mol. Biol. Cell 11 2000 2657 2671
47. --dependent neurotransmitter transporters: drugs, substrates, presynaptic receptors, and signaling systems Pharmacol. Ther. 92 2001 21 55
48. M. Zerial, and H. McBride Rab proteins as membrane organizers Nat. Rev. Mol. Cell Biol. 2 2001 107 117