Organic cation transporter 2 controls brain norepinephrine and serotonin clearance and antidepressant response

Molecular Psychiatry

Volumn 17, Issue 9, 2012, Pages 926-939

  Bacq, A ^a,b,c   Balasse, L ^a,b,c   Biala, G ^d   Guiard, B ^e   Gardier, A M ^e   Schinkel, A ^f   Louis, F ^a,b,c   Vialou, V ^a,b,c,h   Martres, M P ^a,b,c   Chevarin, C ^a,c   Hamon, M ^a,c   Giros, B ^a,b,c,g   Gautron, S ^a,b,c  

^a INSERM   (France)

^b Groupe Enzymologie Moléculaire et Fonctionnelle   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d MEDICAL UNIVERSITY OF LUBLIN   (Poland)

^e University of Paris XI   (France)

^f NETHERLANDS CANCER INSTITUTE   (Netherlands)

^g DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^h MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

aminergic neurotransmission; antidepressant response; depression; mood; organic cation transporter

Indexed keywords

CITALOPRAM; CORTICOSTERONE; NORADRENALIN; ORGANIC CATION TRANSPORTER 2; REBOXETINE; SEROTONIN; VENLAFAXINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; BRAIN TISSUE; CONTROLLED STUDY; DEPRESSION; EX VIVO STUDY; FORCED SWIMMING TEST; FRONTAL CORTEX; GENE DELETION; GENOTYPE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; MOOD; MOUSE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN TARGETING; PSYCHOPHARMACOTHERAPY; TREATMENT RESPONSE; WILD TYPE;

ACTION POTENTIALS; ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; ANXIETY; BRAIN; CORTICOSTERONE; CYCLOHEXANOLS; DEPRESSION; DISEASE MODELS, ANIMAL; FEMALE; HIPPOCAMPUS; LIMBIC SYSTEM; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR IMAGING; NOREPINEPHRINE; ORGANIC CATION TRANSPORT PROTEINS; RADIOLIGAND ASSAY; SEROTONIN;

EID: 84866373794     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2011.87     Document Type: Article

References (66)

1. Torres GE, Gainetdinov RR, Caron MG. Plasma membrane monoamine transporters: structure, regulation and function. Nat Rev Neurosci 2003; 4: 13-25. (Pubitemid 37271085)
2. Iversen L. Neurotransmitter transporters and their impact on the development of psychopharmacology. Br J Pharmacol 2006; 147(Suppl 1): S82-S88. (Pubitemid 43077265)
3. Charney DS. Monoamine dysfunction and the pathophysiology and treatment of depression. J Clin Psychiatry 1998; 59(Suppl 14): 11-14. (Pubitemid 28462383)
4. Manji HK, Drevets WC, Charney DS. The cellular neurobiology of depression. Nat Med 2001; 7: 541-547. (Pubitemid 32448319)
5. Wayment HK, Schenk JO, Sorg BA. Characterization of extracellular dopamine clearance in the medial prefrontal cortex: role of monoamine uptake and monoamine oxidase inhibition. J Neurosci 2001; 21: 35-44. (Pubitemid 32098723)
6. Vizi ES, Zsilla G, Caron MG, Kiss JP. Uptake and release of norepinephrine by serotonergic terminals in norepinephrine transporter knock-out mice: implications for the action of selective serotonin reuptake inhibitors. J Neurosci 2004; 24: 7888-7894. (Pubitemid 39215693)
7. Daws LC, Montanez S, Owens WA, Gould GG, Frazer A, Toney GM et al. Transport mechanisms governing serotonin clearance in vivo revealed by high-speed chronoamperometry. J Neurosci Methods 2005; 143: 49-62. (Pubitemid 40348789)
8. Grundemann D, Schechinger B, Rappold GA, Schomig E. Molecular identification of the corticosterone-sensitive extraneuronal catecholamine transporter. Nat Neurosci 1998; 1: 349-351.
9. Vialou V, Amphoux A, Zwart R, Giros B, Gautron S. Organic cation transporter 3 (Slc22a3) is implicated in salt-intake regulation. J Neurosci 2004; 24: 2846-2851. (Pubitemid 38380963)
10. Amphoux A, Vialou V, Drescher E, Bruss M, Mannoury La Cour C, Rochat C et al. Differential pharmacological in vitro properties of organic cation transporters and regional distribution in rat brain. Neuropharmacology 2006; 50: 941-952. (Pubitemid 43810126)
11. Engel K, Zhou M, Wang J. Identification and characterization of a novel monoamine transporter in the human brain. J Biol Chem 2004; 279: 50042-50049. (Pubitemid 39577815)
12. Zwart R, Verhaagh S, Buitelaar M, Popp-Snijders C, Barlow DP. Impaired activity of the extraneuronal monoamine transporter system known as uptake-2 in Orct3/Slc22a3-deficient mice. Mol Cell Biol 2001; 21: 4188-4196. (Pubitemid 32565301)
13. Jonker JW, Wagenaar E, Van Eijl S, Schinkel AH. Deficiency in the organic cation transporters 1 and 2 (Oct1/Oct2 [Slc22a1/Slc22a2]) in mice abolishes renal secretion of organic cations. Mol Cell Biol 2003; 23: 7902-7908. (Pubitemid 37271485)
14. Vialou V, Balasse L, Callebert J, Launay JM, Giros B, Gautron S. Altered aminergic neurotransmission in the brain of organic cation transporter 3-deficient mice. J Neurochem 2008; 106: 1471-1482.
15. Baganz NL, Horton RE, Calderon AS, Owens WA, Munn JL, Watts LT et al. Organic cation transporter 3: keeping the brake on extracellular serotonin in serotonin-transporter-deficient mice. Proc Natl Acad Sci USA 2008; 105: 18976-18981.
16. Cui M, Aras R, Christian WV, Rappold PM, Hatwar M, Panza J et al. The organic cation transporter-3 is a pivotal modulator of neurodegeneration in the nigrostriatal dopaminergic pathway. Proc Natl Acad Sci USA 2009; 106: 8043-8048.
17. Busch AE, Karbach U, Miska D, Gorboulev V, Akhoundova A, Volk C et al. Human neurons express the polyspecific cation transporter hOCT2, which translocates monoamine neurotransmitters, amantadine, and memantine. Mol Pharmacol 1998; 54: 342-352. (Pubitemid 28368824)
18. Russ H, Engel W, Schomig E. Isocyanines and pseudoisocyanines as a novel class of potent noradrenaline transport inhibitors: synthesis, detection, and biological activity. J Med Chem 1993; 36: 4208-4213. (Pubitemid 24037931)
19. Fabre V, Boutrel B, Hanoun N, Lanfumey L, Fattaccini CM, Demeneix B et al. Homeostatic regulation of serotonergic function by the serotonin transporter as revealed by nonviral gene transfer. J Neurosci 2000; 20: 5065-5075. (Pubitemid 30421710)
20. Kandel ER, Spencer WA, Brinley Jr FJ. Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. J Neurophysiol 1961; 24: 225-242.
21. David DJ, Bourin M, Jego G, Przybylski C, Jolliet P, Gardier AM. Effects of acute treatment with paroxetine, citalopram and venlafaxine in vivo on noradrenaline and serotonin outflow: a microdialysis study in Swiss mice. Br J Pharmacol 2003; 140: 1128-1136. (Pubitemid 37475979)
22. Ordway GA, Stockmeier CA, Cason GW, Klimek V. Pharmacology and distribution of norepinephrine transporters in the human locus coeruleus and raphe nuclei. J Neurosci 1997; 17: 1710-1719. (Pubitemid 27089816)
23. Le Marec N, Hebert C, Amdiss F, Botez MI, Reader TA. Regional distribution of 5-HT transporters in the brain of wild type and 'Purkinje cell degeneration' mutant mice: a quantitative autoradiographic study with [3H]citalopram. J Chem Neuroanat 1998; 15: 155-171. (Pubitemid 28466784)
24. Fabre V, Beaufour C, Evrard A, Rioux A, Hanoun N, Lesch KP et al. Altered expression and functions of serotonin 5-HT1A and 5-HT1B receptors in knock-out mice lacking the 5-HT transporter. Eur J Neurosci 2000; 12: 2299-2310. (Pubitemid 30497028)
25. David DJ, Klemenhagen KC, Holick KA, Saxe MD, Mendez I, Santarelli L et al. Efficacy of the MCHR1 antagonist N-[3-(1-{[4-(3,4-difluorophenoxy)phenyl] methyl}(4-piperidyl))-4-methylphen yl]-2-methylpropanamide (SNAP 94847) in mouse models of anxiety and depression following acute and chronic administration is independent of hippocampal neurogenesis. J Pharmacol Exp Ther 2007; 321: 237-248. (Pubitemid 46456989)
26. Porsolt RD, Le Pichon M, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977; 266: 730-732. (Pubitemid 8073804)
27. David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D, Mendez I et al. Neurogenesis-dependent and-independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 2009; 62: 479-493.
28. LeDoux JE. Emotion circuits in the brain. Annu Rev Neurosci 2000; 23: 155-184.
29. Drevets WC. Prefrontal cortical-amygdalar metabolism in major depression. Ann NY Acad Sci 1999; 877: 614-637. (Pubitemid 29351882)
30. Drevets WC. Neuroimaging studies of mood disorders. Biol Psychiatry 2000; 48: 813-829.
31. Grundemann D, Koster S, Kiefer N, Breidert T, Engelhardt M, Spitzenberger F et al. Transport of monoamine transmitters by the organic cation transporter type 2, OCT2. J Biol Chem 1998; 273: 30915-30920. (Pubitemid 28533093)
32. Gobbi G, Murphy DL, Lesch K, Blier P. Modifications of the serotonergic system in mice lacking serotonin transporters: an in vivo electrophysiological study. J Pharmacol Exp Ther 2001; 296: 987-995. (Pubitemid 32187374)
33. Gourley SL, Wu FJ, Kiraly DD, Ploski JE, Kedves AT, Duman RS et al. Regionally specific regulation of ERK MAP kinase in a model of antidepressant-sensitive chronic depression. Biol Psychiatry 2008; 63: 353-359.
34. Bunin MA, Wightman RM. Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J Neurosci 1998; 18: 4854-4860. (Pubitemid 28285394)
35. Mundorf ML, Joseph JD, Austin CM, Caron MG, Wightman RM. Catecholamine release and uptake in the mouse prefrontal cortex. J Neurochem 2001; 79: 130-142. (Pubitemid 32946650)
36. Mitchell K, Oke AF, Adams RN. In vivo dynamics of norepinephrine release-reuptake in multiple terminal field regions of rat brain. J Neurochem 1994; 63: 917-926. (Pubitemid 24266604)
37. Bengel D, Murphy DL, Andrews AM, Wichems CH, Feltner D, Heils A et al. Altered brain serotonin homeostasis and locomotor insensitivity to 3, 4-methylenedioxymethamphetamine ('Ecstasy') in serotonin transporter-deficient mice. Mol Pharmacol 1998; 53: 649-655. (Pubitemid 28196486)
38. Xu F, Gainetdinov RR, Wetsel WC, Jones SR, Bohn LM, Miller GW et al. Mice lacking the norepinephrine transporter are supersensitive to psychostimulants. Nat Neurosci 2000; 3: 465-471. (Pubitemid 30495628)
39. Sheline YI. Neuroimaging studies of mood disorder effects on the brain. Biol Psychiatry 2003; 54: 338-352. (Pubitemid 37267862)
40. Rajkowska G. Postmortem studies in mood disorders indicate altered numbers of neurons and glial cells. Biol Psychiatry 2000; 48: 766-777.
41. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005; 45: 651-660. (Pubitemid 40320700)
42. Tremblay P, Blier P. Catecholaminergic strategies for the treatment of major depression. Curr Drug Targets 2006; 7: 149-158.
43. Lin CJ, Tai Y, Huang MT, Tsai YF, Hsu HJ, Tzen KY et al. Cellular localization of the organic cation transporters, OCT1 and OCT2, in brain microvessel endothelial cells and its implication for MPTP transport across the blood-brain barrier and MPTP-induced dopaminergic toxicity in rodents. J Neurochem 2010; 114: 717-727.
44. Roche M, Commons KG, Peoples A, Valentino RJ. Circuitry underlying regulation of the serotonergic system by swim stress. J Neurosci 2003; 23: 970-977. (Pubitemid 36206188)
45. Heisler LK, Pronchuk N, Nonogaki K, Zhou L, Raber J, Tung L et al. Serotonin activates the hypothalamic-pituitary-adrenal axis via serotonin 2C receptor stimulation. J Neurosci 2007; 27: 6956-6964. (Pubitemid 47015900)
46. Radley JJ, Williams B, Sawchenko PE. Noradrenergic innervation of the dorsal medial prefrontal cortex modulates hypothalamopituitary-adrenal responses to acute emotional stress. J Neurosci 2008; 28: 5806-5816.
47. Ulrich-Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 2009; 10: 397-409.
48. Linthorst AC, Penalva RG, Flachskamm C, Holsboer F, Reul JM. Forced swim stress activates rat hippocampal serotonergic neurotransmission involving a corticotropin-releasing hormone receptor-dependent mechanism. Eur J Neurosci 2002; 16: 2441-2452. (Pubitemid 36056968)
49. Ma S, Morilak DA. Norepinephrine release in medial amygdala facilitates activation of the hypothalamic-pituitary-adrenal axis in response to acute immobilisation stress. J Neuroendocrinol 2005; 17: 22-28. (Pubitemid 40360971)
50. Yoshitake T, Wang FH, Kuteeva E, Holmberg K, Yamaguchi M, Crawley JN et al. Enhanced hippocampal noradrenaline and serotonin release in galanin-overexpressing mice after repeated forced swimming test. Proc Natl Acad Sci USA 2004; 101: 354-359. (Pubitemid 38084254)
51. Schreiber R, Brocco M, Gobert A, Veiga S, Millan MJ. The potent activity of the 5-HT1A receptor agonists, S 14506 and S 14671, in the rat forced swim test is blocked by novel 5-HT1A receptor antagonists. Eur J Pharmacol 1994; 271: 537-541.
52. De Vry J, Schreiber R, Melon C, Dalmus M, Jentzsch KR. 5-HT1A receptors are differentially involved in the anxiolytic-and antidepressant-like effects of 8-OH-DPAT and fluoxetine in the rat. Eur Neuropsychopharmacol 2004; 14: 487-495. (Pubitemid 39626897)
53. File SE, Gonzalez LE, Andrews N. Comparative study of pre-and postsynaptic 5-HT1A receptor modulation of anxiety in two ethological animal tests. J Neurosci 1996; 16: 4810-4815. (Pubitemid 26251075)
54. Savitz J, Lucki I, Drevets WC. 5-HT(1A) receptor function in major depressive disorder. Prog Neurobiol 2009; 88: 17-31.
55. Li Q, Wichems C, Heils A, Lesch KP, Murphy DL. Reduction in the density and expression, but not G-protein coupling, of serotonin receptors (5-HT1A) in 5-HT transporter knock-out mice: gender and brain region differences. J Neurosci 2000; 20: 7888-7895.
56. Koepsell H, Lips K, Volk C. Polyspecific organic cation transporters: structure, function, physiological roles, and biopharmaceutical implications. Pharm Res 2007; 24: 1227-1251. (Pubitemid 46876495)
57. Blier P, Pineyro G, el Mansari M, Bergeron R, de Montigny C. Role of somatodendritic 5-HT autoreceptors in modulating 5-HT neurotransmission. Ann NYAcad Sci 1998; 861: 204-216. (Pubitemid 29047718)
58. Cremers TI, de Boer P, Liao Y, Bosker FJ, den Boer JA, Westerink BH et al. Augmentation with a 5-HT(1A), but not a 5-HT(1B) receptor antagonist critically depends on the dose of citalopram. Eur J Pharmacol 2000; 397: 63-74. (Pubitemid 30323812)
59. Detke MJ, Wieland S, Lucki I. Blockade of the antidepressant-like effects of 8-OH-DPAT, buspirone and desipramine in the rat forced swim test by 5HT1A receptor antagonists. Psychopharmacology (Berl) 1995; 119: 47-54.
60. Surget A, Saxe M, Leman S, Ibarguen-Vargas Y, Chalon S, Griebel G et al. Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol Psychiatry 2008; 64: 293-301.
61. Kobayashi K, Ikeda Y, Sakai A, Yamasaki N, Haneda E, Miyakawa T et al. Reversal of hippocampal neuronal maturation by serotonergic antidepressants. Proc Natl Acad Sci USA 2010; 107: 8434-8439.
62. Yanpallewar SU, Fernandes K, Marathe SV, Vadodaria KC, Jhaveri D, Rommelfanger K et al. Alpha2-adrenoceptor blockade accelerates the neurogenic, neurotrophic, and behavioral effects of chronic antidepressant treatment. J Neurosci 2010; 30: 1096-1109.
63. Richardson-Jones JW, Craige CP, Guiard BP, Stephen A, Metzger KL, Kung HF et al. 5-HT1A autoreceptor levels determine vulnerability to stress and response to antidepressants. Neuron 2010; 65: 40-52.
64. Beique J, de Montigny C, Blier P, Debonnel G. Effects of sustained administration of the serotonin and norepinephrine reuptake inhibitor venlafaxine: I. in vivo electrophysiological studies in the rat. Neuropharmacology 2000; 39: 1800-1812. (Pubitemid 30398484)
65. Szabo ST, Blier P. Effects of the selective norepinephrine reuptake inhibitor reboxetine on norepinephrine and serotonin transmission in the rat hippocampus. Neuropsychopharmacology 2001; 25: 845-857. (Pubitemid 34031891)
66. Berrocoso E, Mico JA. In vivo effect of venlafaxine on locus coeruleus neurons: role of opioid, alpha(2)-adrenergic, and 5-hydroxytryptamine(1A) receptors. J Pharmacol Exp Ther 2007; 322: 101-107. (Pubitemid 46956369)