Serotonin transport and serotonin transporter-mediated antidepressant recognition are controlled by 5-HT2B receptor signaling in serotonergic neuronal cells

FASEB Journal

Volumn 20, Issue 11, 2006, Pages 1843-1854

  Launay, Jean Marie ^a,e   Schneider, Benoit ^b,c   Loric, Sylvain ^b,c   Da Prada, Mose ^d   Kellermann, Odile ^b,c  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b INSTITUT ANDRÉ LWOFF   (France)

^c INSTITUT PASTEUR   (France)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

^e HÔPITAL LARIBOISIÈRE   (France)

Author keywords

Neuronal differentiation; SERT; Transporter(s)

Indexed keywords

3BETA (4 IODOPHENYL) 2BETA TROPANECARBOXYLIC ACID METHYL ESTER; 4 (5,6 DIMETHYL 2 BENZOFURANYL)PIPERIDINE; 6 NITROQUIPAZINE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AMITRIPTYLINE; ANTIDEPRESSANT AGENT; CIANOPRAMINE; CITALOPRAM; CLOMIPRAMINE; COCAINE; DESIPRAMINE; DICLOFENSINE; FLUOXETINE; IMIPRAMINE; INDALPINE; NITRIC OXIDE; NOMIFENSINE; PAROXETINE; POLYADENYLIC ACID; SEROTONIN; SEROTONIN 2B RECEPTOR; SEROTONIN TRANSPORTER; MESSENGER RNA; TRICYCLIC ANTIDEPRESSANT AGENT;

ALPHA CHAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG BINDING; DRUG MECHANISM; ENZYME PHOSPHORYLATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA TRANSLATION; SEROTONIN UPTAKE; SEROTONINERGIC NERVE CELL; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL MEMBRANE; CYTOLOGY; DRUG EFFECT; FRONTAL LOBE; GENETICS; METABOLISM; NERVE CELL; PHOSPHORYLATION; PHYSIOLOGY; RAPHE NUCLEUS; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ANTIDEPRESSIVE AGENTS, TRICYCLIC; BIOLOGICAL TRANSPORT; CELL DIFFERENTIATION; CELL MEMBRANE; CELLS, CULTURED; FRONTAL LOBE; MALE; MICE; MICE, INBRED BALB C; NEURONS; PHOSPHORYLATION; RAPHE NUCLEI; RECEPTOR, SEROTONIN, 5-HT2B; RNA, MESSENGER; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SIGNAL TRANSDUCTION;

EID: 33748648565     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-5724com     Document Type: Article

References (62)

1. Hoyer, D., Hannon, J. P., and Martin, G. R. (2002) Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol. Biochem. Behav. 71, 533-554
2. Rudnick, G., and Clark, J. (1993) From synapse to vesicle: the reuptake and storage of biogenic amine neurotransmitters. Biochim. Biophys. Acta 1144, 249-263
3. - neurotransmitter transporters. J. Neurochem. 71, 1785-1803
4. Akunne, H. C., de Costa, B. R., Jacobson, A. E., Rice, K. C., and Rothman, R. B. (1992) [3H] cocaine labels a binding site associated with the serotonin transporter in guinea pig brain: allosteric modulation by paroxetine. Neurochem. Res. 17, 1275-1283
5. Rudnick, G., and Wall, S. C. (1992) The molecular mechanism of "ecstasy" [3,4-methylenedioxy-methamphetamine (MDMA)]: serotonin transporters are targets for MDMA-induced serotonin release. Proc. Natl. Acad. Sci. U. S. A. 89, 1817-1821
6. Marcusson, J. O., and Ross, S. B. (1990) Binding of some antidepressants to the 5-HT transporter in brain and platelets. Psychopharmacology (Berlin) 102, 145-155
7. Schloss, P., and Betz, H. (1995) Heterogeneity of antidepressant binding sites on the recombinant rat serotonin transporter SERT1. Biochemistry 34, 12590-12595
8. Svenningsson, P., Chergui, K., Rachleff, I., Flajolet, M., Zhang, X., Yacoubi, M. E., Vaugeois, J. M., Nomikos, G. G., and Greengard, P. (2006) Alterations in 5-HT1B receptor function by p11 in depression-like states. Science 311, 77-80
9. Owens, M. J., and Nemeroff, C. B. (1994) Role of serotonin in the pathophysiology of depression: focus on the serotonin transporter. Clin. Chem. 40, 288-295
10. Lieberman, J. A., Mailman, R. B., Duncan, G., Sikich, L., Chakos, M., Nichols, D. E., and Kraus, J. E. (1998) Serotonergic basis of antipsychotic drug effects in schizophrenia. Biol. Psychiatry 44, 1099-1117
11. White, K. J., Walline, C. C., and Barker, E. L. (2005) Serotonin transporters: implications for antidepressant drug development. AAPS J. 7, E421-433
12. Tuomisto, J., and Tukiainen, E. (1976) Decreased uptake of 5-HT in blood platelets from depressed patients. Nature 262, 596-598
13. Briley, M. S., Langer, S. Z., Raisman, R., Sechter, D., and Zarifian, E. (1980) Tritiated imipramine binding sites are decreased in platelets of untreated depressed patients. Science 209, 303-305
14. Da Prada, M., Cesura, A. M., Launay, J. M., and Richards, J. G. (1988) Platelets as a model for neurones? Experientia 44, 115-126
15. Lesch, K. P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., Benjamin, J., Muller, C. R., Hamer, D. H., and Murphy, D. L. (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531
16. Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., and Poulton, R. (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386-389
17. Hoffman, B. J., Mezey, E., and Brownstein, M. J. (1991) Cloning of a serotonin transporter affected by antidepressants. Science 254, 579-580
18. Blakely, R. D., Berson, H. E., Fremeau, R. T., Jr., Caron, M. G., Peek, M. M., Prince, H. K., Bradley, C. C., Hoffman, B. J., Mezey, E., and Brownstein, M. J. (1991) Cloning and expression of a functional serotonin transporter from rat brain. Nature 354, 66-70
19. Ramamoorthy, S., Bauman, A. L., Moore, K. R., Han, H., Yang-Feng, T., Chang, A. S., Ganapathy, V., and Blakely, R. D. (1993) Antidepressant- and cocaine-sensitive human serotonin transporter: molecular cloning, expression, and chromosomal localization. Proc. Natl. Acad. Sci. U. S. A. 90, 2542-2546
20. Launay, J. M., Geoffroy, C., Mutel, V., Buckle, M., Cesura, A., Alouf, J. E., and Da Prada, M. (1992) One-step purification of the serotonin transporter located at the human platelet plasma membrane. J. Biol. Chem. 267, 11344-11351
21. Rotondo, A., Giannaccini, G., Betti, L., Chiellini, G., Marazziti, D., Martin, C., Lucacchini, A., and Cassano, G. B. (1996) The serotonin transporter from human brain: purification and partial characterization. Neurochem. Int. 28, 299-307
22. Launay, J. M., Bondoux, D., Oset-Gasque, M. J., Emami, S., Mutel, V., Haimart, M., and Gespach, C. (1994) Increase of human platelet serotonin uptake by atypical histamine receptors. Am. J. Physiol. 266, R526-R536
23. Miller, K. J., and Hoffman, B. J. (1994) Adenosine A3 receptors regulate serotonin transport via nitric oxide and cGMP. J. Biol. Chem. 269, 27351-27356
24. Zhu, C. B., Hewlett, W. A., Feoktistov, I., Biaggioni, I., and Blakely, R. D. (2004) Adenosine receptor, protein kinase G, and p38 mitogen-activated protein kinase-dependent up-regulation of serotonin transporters involves both transporter trafficking and activation. Mol. Pharmacol. 65, 1462-1474
25. Torres, G. E., Gainetdinov, R. R., and Caron, M. G. (2003) Plasma membrane monoamine transporters: structure, regulation and function. Nat. Rev. Neurosci. 4, 13-25
26. Buc-Caron, M. H., Launay, J. M., Lamblin, D., and Kellermann, O. (1990) Serotonin uptake, storage, and synthesis in an immortalized committed cell line derived from mouse teratocarcinoma. Proc. Natl. Acad. Sci. U. S. A. 87, 1922-1926
27. Mouillet-Richard, S., Mutel, V., Loric, S., Tournois, C., Launay, J. M., and Kellermann, O. (2000) Regulation by neurotransmitter receptors of serotonergic or catecholaminergic neuronal cell differentiation. J. Biol. Chem. 275, 9186-9192
28. Kellermann, O., Loric, S., Maroteaux, L., and Launay, J. M. (1996) Sequential onset of three 5-HT receptors during the 5-HTrgic differentiation of the murine 1C11 cell line. Br. J. Pharmacol. 118, 1161-1170
29. Agrez, M. V., Ames, M. M., Lieber, M. M., and Tyce, G. M. (1984) The presence of serotonin in animal sera used in cell culture. Biog. Amines. 1, 223-228
30. Walker, R. F., Friedman, D. W., and Jimenez, A. (1983) A modified enzymatic-isotopic microassay for serotonin (5HT) using 5HT-N-acetyltransferase partially purified from Drosophila. Life Sci. 33, 1915-1924
31. Gray, E. G., and Whittaker, V. P. (1962) The isolation of nerve endings from brain: an electron-microscopic study of cell fragments derived by homogenization and centrifugation. J. Anat. 96, 79-88
32. O'Reilly, C. A., and Reith, M. E. (1988) Uptake of [3H]serotonin into plasma membrane vesicles from mouse cerebral cortex. J. Biol. Chem. 263, 6115-6121
33. Brewer, G. J. (1995) Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J. Neurosci. Res. 42, 674-683
34. Loric, S., Maroteaux, L., Kellermann, O., and Launay, J. M. (1995) Functional serotonin-2B receptors are expressed by a teratocarcinoma-derived cell line during serotoninergic differentiation. Mol. Pharmacol. 47, 458-466
35. Perrella, F. W. (1988) EZ-FIT: a practical curve-fitting microcomputer program for the analysis of enzyme kinetic data on IBM-PC compatible computers. Anal. Biochem. 174, 437-447
36. Poliard, A., Lamblin, D., Marie, P. J., Buc-Caron, M. H., and Kellermann, O. (1993) Commitment of the teratocarcinoma-derived mesodermal clone C1 towards terminal osteogenic differentiation. J. Cell Sci. 106, 503-512
37. Salles, F. J., Darrow, A. L., O'Connell, M. L., and Strickland, S. (1992) Isolation of novel murine maternal mRNAs regulated by cytoplasmic polyadenylation. Genes Dev. 6, 1202-1212
38. Doucet, A., Katz, A. I., and Morel, F. (1979) Determination of Na-K-ATPase activity in single segments of the mammalian nephron. Am. J. Physiol. 237, F105-F113
39. Celsi, G., Nishi, A., Akusjarvi, G., and Aperia, A. (1991) Abundance of Na(+)-K(+)-ATPase mRNA is regulated by glucocorticoid hormones in infant rat kidneys. Am. J. Physiol. 260, F192-F197
40. Groisman, I., Jung, M. Y., Sarkissian, M., Cao, Q., and Richter, J. D. (2002) Translational control of the embryonic cell cycle. Cell. 109, 473-483
41. Read, R. L., and Norbury, C. J. (2002) Roles for cytoplasmic polyadenylation in cell cycle regulation. J. Cell. Biochem. 87, 258-265
42. Sarrias, M. J., Cabre, P., Martinez, E., and Artigas, F. (1990) Relationship between serotoninergic measures in blood and cerebrospinal fluid simultaneously obtained in humans. J. Neurochem. 54, 783-786
43. Beck, O., Wallen, N. H., Broijersen, A., Larsson, P. T., and Hjemdahl, P. (1993) On the accurate determination of serotonin in human plasma. Biochem. Biophys. Res. Commun. 196, 260-266
44. Audia, J. E., Evrard, D. A., Murdoch, G. R., Droste, J. J., Nissen, J. S., Schenck, K. W., Fludzinski, P., Lucaites, V. L., Nelson, D. L., and Cohen, M. L. (1996) Potent, selective tetrahydro-betacarboline antagonists of the serotonin 2B (5HT2B) contractile receptor in the rat stomach fundus. J. Med. Chem. 39, 2773-2780
45. Bertorello, A. M., Aperia, A., Walaas, S. I., Nairn, A. C., and Greengard, P. (1991) Phosphorylation of the catalytic subunit of Na+,K(+)-ATPase inhibits the activity of the enzyme. Proc. Natl. Acad. Sci. U. S. A. 88, 11359-11362
46. Logvinenko, N. S., Dulubova, I., Fedosova, N., Larsson, S. H., Nairn, A. C., Esmann, M., Greengard, P., and Aperia, A. (1996) Phosphorylation by protein kinase C of serine-23 of the alpha-1 subunit of rat Na+,K(+)-ATPase affects its conformational equilibrium. Proc. Natl. Acad. Sci. U. S. A. 93, 9132-9137
47. Therien, A. G., and Blostein, R. (2000) Mechanisms of sodium pump regulation. Am. J. Physiol. 279, C541-C566
48. Launay, J. M., Birraux, G., Bondoux, D., Callebert, J., Choi, D. S., Loric, S., and Maroteaux, L. (1996) Ras involvement in signal transduction by the serotonin 5-HT2B receptor. J. Biol. Chem. 271, 3141-3147
49. Manivet, P., Mouillet-Richard, S., Callebert, J., Nebigil, C. G., Maroteaux, L., Hosoda, S., Kellermann, O., and Launay, J. M. (2000) PDZ-dependent activation of nitric-oxide synthases by the serotonin 2B receptor. J. Biol. Chem. 275, 9324-9331
50. Bonaventure, P., Guo, H., Tian, B., Liu, X., Bittner, A., Roland, B., Salunga, R., Ma, X. J., Kamme, F., and Meurers, B., et al. (2002) Nuclei and subnuclei gene expression profiling in mammalian brain. Brain Res. 943, 38-47
51. Vandenbergh, D. J., Mori, N., and Anderson, D. J. (1991) Co-expression of multiple neurotransmitter enzyme genes in normal and immortalized sympathoadrenal progenitor cells. Dev. Biol. 148, 10-22
52. Ramamoorthy, S., and Blakely, R. D. (1999) Phosphorylation and sequestration of serotonin transporters differentially modulated by psychostimulants. Science 285, 763-766
53. Vaughan, R. A. (2004) Phosphorylation and regulation of psychostimulant-sensitive neurotransmitter transporters. J. Pharmacol. Exp. Ther. 310, 1-7
54. Zhang, Y. W., and Rudnick, G. (2005) Serotonin transporter mutations associated with obsessive-compulsive disorder and phosphorylation alter binding affinity for inhibitors. Neuropharmacology 49, 791-797
55. Wong, M. L., and Licinio, J. (2001) Research and treatment approaches to depression. Nat. Rev. Neurosci. 2, 343-351
56. Catterall, W., and Mackie, M. (2001) Local Anesthetics, McGraw-Hill, New York
57. Lauder, J. M., Wallace, J. A., Wilkie, M. B., DiNome, A., and Krebs, H. (1983) Roles for serotonin in neurogenesis. Monogr. Neural. Sci. 9, 3-10
58. Gaspar, P., Cases, O., and Maroteaux, L. (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat. Rev. Neurosci. 4, 1002-1012
59. Shuey, D. L., Sadler, T. W., and Lauder, J. M. (1992) Serotonin as a regulator of craniofacial morphogenesis: site specific malformations following exposure to serotonin uptake inhibitors. Teratology 46, 367-378
60. Jacobs, B. L., Tanapat, P., Reeves, A., and Gould, E. (1998) Serotonin stimulates the production of new hippocampal granule neurons via the 5-HT1A receptor in the adult rat. Soc. Neurosci. Abstr. 23, 1992
61. Malberg, J. E., Eisch, A. J., Nestler, E. J., and Duman, R. S. (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20, 9104 -9110
62. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., and Arancio, O., et al. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809