Corticosterone-sensitive monoamine transport in the rat dorsomedial hypothalamus: Potential role for organic cation transporter 3 in stress-induced modulation of monoaminergic neurotransmission

Journal of Neuroscience

Volumn 26, Issue 34, 2006, Pages 8758-8766

  Gasser, Paul J ^a,b   Lowry, Christopher A ^b   Orchinik, Miles ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Corticosterone; Monoamine; Organic cation transporter; Serotonin; Stress; Uptake

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; CORTICOSTERONE; DECYNIUM22; DOPAMINE; ESTRADIOL; HISTAMINE; MONOAMINE; NORADRENALIN; ORGANIC CATION TRANSPORTER; PROTEIN INHIBITOR; SEROTONIN; UNCLASSIFIED DRUG;

AMINE TRANSPORT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; DOSE RESPONSE; EXPERIMENTAL MODEL; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MONOAMINERGIC SYSTEM; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEROTONIN UPTAKE; SEROTONINERGIC SYSTEM; STRESS;

1-METHYL-4-PHENYLPYRIDINIUM; ANIMALS; BIOGENIC MONOAMINES; BIOLOGICAL TRANSPORT; CORTICOSTERONE; HISTAMINE; HYPOTHALAMUS; MALE; ORGANIC CATION TRANSPORT PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; STRESS; SYNAPTIC TRANSMISSION; TISSUE DISTRIBUTION;

EID: 33748264554     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0570-06.2006     Document Type: Article

References (73)

1. Abercrombie ED, Jacobs BL (1987) Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressful and nonstressful stimuli. J Neurosci 7:2837-2843.
2. Amphoux A, Vialou V, Drescher E, Bruss M, La Cour CM, Rochat C, Millan MJ, Giros B, Bonisch H, Gautron S (2006) Differential pharmacological in vitro properties of organic cation transporters and regional distribution in rat brain. Neuropharmacology 50:941-952.
3. Arndt P, Volk C, Gorboulev V, Budiman T, Popp C, Ulzheimer-Teuber I, Akhoundova A, Koppatz S, Bamberg E, Nagel G, Koepsell H (2001) Interaction of cations, anions, and weak base quinine with rat renal cation transporter rOCT2 compared with rOCT1. Am J Physiol Renal Physiol 281:F454-F468.
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
5. Busch AE, Quester S, Ulzheimer JC, Gorboulev V, Akhoundova A, Waldegger S, Lang F, Koepsell H (1996) Monoamine neurotransmitter transport mediated by the polyspecific cation transporter rOCT1. FEBS Lett 395:153-156.
6. Busch AE, Karbach U, Miska D, Gorboulev V, Akhoundova A, Volk C, Arndt P, Ulzheimer JC, Sonders MS, Baumann C, Waldegger S, Lang F, Koepsell H (1998) Human neurons express the polyspecific cation transporter hOCT2, which translocates monoamine neurotransmitters, amantadine, and memantine. Mol Pharmacol 54:342-352.
7. Clark MS, Russo AF (1997) Tissue-specific glucocorticoid regulation of tryptophan hydroxylase mRNA levels. Brain Res Mol Brain Res 48:346-354.
8. Corbel S, Dy M (1996) Evidence for bidirectional histamine transport by murine hematopoietic progenitor cells. FEBS Lett 391:279-281.
9. Daugherty WP, Corley KC, Phan TH, Boadle-Biber MC (2001) Further studies on the activation of rat median raphe serotonergic neurons by inescapable sound stress. Brain Res 923:103-111.
10. Deakin JF (1998) The role of serotonin in panic, anxiety and depression. Int Clin Psychopharmacol 13 [Suppl 4]:S1-S5.
11. Dimaline R, Struthers J (1996) Expression and regulation of a vesicular monoamine transporter in rat stomach: a putative histamine transporter. J Physiol Lond 490:249-256.
12. DiMicco JA, Samuels BC, Zaretskaia MV, Zaretsky DV (2002) The dorsomedial hypothalamus and the response to stress: part renaissance, part revolution. Pharmacol Biochem Behav 71:469-480.
13. Ekblom J, Jossan SS, Bergstrom M, Oreland L, Walum E, Aquilonius SM (1993) Monoamine oxidase-B in astrocytes. Glia 8:122-132.
14. Engel K, Zhou M, Wang J (2004) Identification and characterization of a novel monoamine transporter in the human brain. J Biol Chem 279:50042-50049.
15. Feng N, Mo B, Johnson PL, Orchinik M, Lowry CA, Renner KJ (2005) Local inhibition of organic cation transporters increases extracellular serotonin in the medial hypothalamus. Brain Res 1063:69-76.
16. Gasser PJ, Lowry CA, Renner KJ, Orchinik M (2004) Expression and function of organic cation transporters in the rat dorsomedial hypothalamus. Soc Neurosci Abstr 30:1000.9.
17. Gasser PJ, Lowry CA, Orchinik M (2005) Corticosterone-sensitive monoamine transport in the rat dorsomedial hypothalamus: role for organic cation transporter 3 in stress-induced serotonin accumulation. Soc Neurosci Abstr 31:872.12.
18. Graeff FG, Guimaraes FS, De Andrade TG, Deakin JF (1996) Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 54:129-141.
19. Grundemann D, Gorboulev V, Gambaryan S, Veyhl M, Koepsell H (1994) Drug excretion mediated by a new prototype of polyspecific transporter. Nature 372:549-552.
20. Grundemann D, Koster S, Kiefer N, Breidert T, Engelhardt M, Spitzenberger F, Obermuller N, Schomig E (1998) Transport of monoamine transmitters by the organic cation transporter type 2, OCT2. J Biol Chem 273:30915-30920.
21. Grundemann D, Liebich G, Kiefer N, Koster S, Schomig E (1999) Selective substrates for non-neuronal monoamine transporters. Mol Pharmacol 56:1-10.
22. Haag C, Berkels R, Grundemann D, Lazar A, Taubert D, Schomig E (2004) The localisation of the extraneuronal monoamine transporter (EMT) in rat brain. J Neurochem 88:291-297.
23. Hayashi M, Haga M, Yatsushiro S, Yamamoto A, Moriyama Y (1999) Vesicular monoamine transporter 1 is responsible for storage of 5-hydroxytryptamine in rat pinealocytes. J Neurochem 73:2538-2545.
24. Inazu M, Kubota N, Takeda H, Zhang J, Kiuchi Y, Oguchi K, Matsumiya T (1999) Pharmacological characterization of dopamine transport in cultured rat astrocytes. Life Sci 64:2239-2245.
25. Inazu M, Takeda H, Ikoshi H, Sugisawa M, Uchida Y, Matsumiya T (2001) Pharmacological characterization and visualization of the glial serotonin transporter. Neurochem Int 39:39-49.
26. Inazu M, Takeda H, Matsumiya T (2003a) Expression and functional characterization of the extraneuronal monoamine transporter in normal human astrocytes. J Neurochem 84:43-52.
27. Inazu M, Takeda H, Matsumiya T (2003b) Functional expression of the norepinephrine transporter in cultured rat astrocytes. J Neurochem 84:136-144.
28. Jonker JW, Schinkel AH (2004) Pharmacological and physiological functions of the polyspecific organic cation transporters: OCT1, 2, and 3 (SLC22A1-3). J Pharmacol Exp Ther 308:2-9.
29. Kitaichi K, Morishita Y, Doi Y, Ueyama J, Matsushima M, Zhao YL, Takagi K, Hasegawa T (2003) Increased plasma concentration and brain penetration of methamphetamine in behaviorally sensitized rats. Eur J Pharmacol 464:39-48.
30. Koepsell H, Schmitt BM, Gorboulev V (2003) Organic cation transporters. Rev Physiol Biochem Pharmacol 150:36-90.
31. Kovacs GL, Telegdy G (1980) Influence of corticosterone on serotonin metabolism in rat brain. Neurosci Behav Physiol 10:232-236.
32. Kristufek D, Rudorfer W, Pifl C, Huck S (2002) Organic cation transporter mRNA and function in the rat superior cervical ganglion. J Physiol (Lond) 543:117-134.
33. Kvetnansky R, Palkovits M, Mitro A, Torda T, Mikulaj L (1977) Catecholamines in individual hypothalamic nuclei of acutely and repeatedly stressed rats. Neuroendocrinology 23:257-267.
34. Levi G, Raiteri M (1993) Carrier-mediated release of neurotransmitters. Trends Neurosci 16:415-419.
35. Lips KS, Volk C, Schmitt BM, Pfeil U, Arndt P, Miska D, Ermert L, Kummer W, Koepsell H (2005) Polyspecific cation transporters mediate luminal release of acetylcholine from bronchial epithelium. Am J Respir Cell Mol Biol 33:79-88.
36. Losada MEO (1988) Corticosterone-induced acute changes on biogenic amines levels in some areas of the rat brain. Biog Amines 5:239-247.
37. Lowry CA (2002) Functional subsets of serotonergic neurones: implications for control of the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 14:911-923.
38. Lowry CA, Burke KA, Renner KJ, Moore FL, Orchinik M (2001) Rapid changes in monoamine levels following administration of corticotropin-releasing factor or corticosterone are localized in the dorsomedial hypothalamus. Horm Behav 39:195-205.
39. Lowry CA, Plant A, Shanks N, Ingram CD, Lightman SL (2003) Anatomical and functional evidence for a stress-responsive, monoamine-accumulating area in the dorsomedial hypothalamus of adult rat brain. Horm Behav 43:254-262.
40. Martel F, Martins MJ, Azevedo I (1996) Inward transport of 3H-MPP+ in freshly isolated rat hepatocytes: evidence for interaction with catecholamines. Naunyn Schmiedebergs Arch Pharmacol 354:305-311.
41. Meijer OC, de Kloet ER (1998) Corticosterone and serotonergic neurotransmission in the hippocampus: functional implications of central corticosteroid receptor diversity. Crit Rev Neurobiol 12:1-20.
42. Merickel A, Edwards RH (1995) Transport of histamine by vesicular monoamine transporter-2. Neuropharmacology 34:1543-1547.
43. Neckers L, Sze PY (1975) Regulation of 5-hydroxytryptamine metabolism in mouse brain by adrenal glucocorticoids. Brain Res 93:123-132.
44. Okuda M, Saito H, Urakami Y, Takano M, Inui K (1996) cDNA cloning and functional expression of a novel rat kidney organic cation transporter, OCT2. Biochem Biophys Res Commun 224:500-507.
45. Okuda M, Urakami Y, Saito H, Inui K (1999) Molecular mechanisms of organic cation transport in OCT2-expressing Xenopus oocytes. Biochim Biophys Acta 1417:224-231.
46. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. San Diego: Academic.
47. Reed B, Chen N, Justice Jr JB (2003) Dual-electrode voltammetry of catecholamine transport: simultaneous monitoring of uptake and efflux. J Neurosci Methods 126:127-135.
48. Russ H, Gliese M, Sonna J, Schomig E (1992) The extraneuronal transport mechanism for noradrenaline (uptake2) avidly transports 1-methyl-4- phenylpyridinium (MPP+). Naunyn Schmiedebergs Arch Pharmacol 346:158-165.
49. Russ H, Sonna J, Keppler K, Baunach S, Schomig E (1993) Cyanine-related compounds: a novel class of potent inhibitors of extraneuronal noradrenaline transport. Naunyn Schmiedebergs Arch Pharmacol 348:458-465.
50. Russ H, Staust K, Martel F, Gliese M, Schomig E (1996) The extraneuronal transporter for monoamine transmitters exists in cells derived from human central nervous system glia. Eur J Neurosci 8:1256-1264.
51. Saphier D, Farrar GE, Welch JE (1995) Differential inhibition of stress-induced adrenocortical responses by 5-HT1A agonists and by 5-HT2 and 5-HT3 antagonists. Psychoneuroendocrinology 20:239-257.
52. Saphier D, Welch JE (1995) Effects of the serotonin1A agonist, 8-hydroxy-2-(di-n-propylamino)tetralin on neurochemical responses to stress. J Neurochem 64:767-776.
53. Sayre LM (1989) Biochemical mechanism of action of the dopaminergic neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Toxicol Lett 48:121-149.
54. Scholze P, Norregaard L, Singer EA, Freissmuth M, Gether U, Sitte HH (2002) The role of zinc ions in reverse transport mediated by monoamine transporters. J Biol Chem 277:21505-21513.
55. Schomig E, Russ H, Staudt K, Martel F, Gliese M, Grundemann D (1998) The extraneuronal monoamine transporter exists in human central nervous system glia. Adv Pharmacol 42:356-359.
56. Shang T, Uihlein AV, Van Asten J, Kalyanaraman B, Hillard CJ (2003) 1-Methyl-4-phenylpyridinium accumulates in cerebellar granule neurons via organic cation transporter 3. J Neurochem 85:358-367.
57. Shekhar A, Katner JS, Sajdyk TJ, Kohl RR (2002) Role of norepinephrine in the dorsomedial hypothalamic panic response: an in vivo microdialysis study. Pharmacol Biochem Behav 71:493-500.
58. Singh VB, Corley KC, Phan TH, Boadle-Biber MC (1990) Increases in the activity of tryptophan hydroxylase from rat cortex and midbrain in response to acute or repeated sound stress are blocked by adrenalectomy and restored by dexamethasone treatment. Brain Res 516:66-76.
59. Slitt AL, Cherrington NJ, Hartley DP, Leazer TM, Klaassen CD (2002) Tissue distribution and renal developmental changes in rat organic cation transporter mRNA levels. Drug Metab Dispos 30:212-219.
60. Summers CH, Larson ET, Ronan PJ, Hofmann PM, Emerson AJ, Renner KJ (2000) Serotonergic responses to corticosterone and testosterone in the limbic system. Gen Comp Endocrinol 117:151-159.
61. Summers TR, Matter JM, McKay JM, Ronan PJ, Larson ET, Renner KJ, Summers CH (2003) Rapid glucocorticoid stimulation and GABAergic inhibition of hippocampal serotonergic response: in vivo dialysis in the lizard anolis carolinensis. Horm Behav 43:245-253.
62. Swanson LW (1987) The hypothalamus. In: Handbook of Chemical Neuroanatomy (Bjorklund A, Hokfelt T, Swanson LW, eds), pp 1-104. Amsterdam: Elsevier.
63. Sze PY (1976) Glucocorticoid regulation of the serotonergic system of the brain. Adv Biochem Psychopharmacol 15:251-265.
64. Takeda H, Inazu M, Matsumiya T (2002) Astroglial dopamine transport is mediated by norepinephrine transporter. Naunyn Schmiedebergs Arch Pharmacol 366:620-623.
65. Verhaagh S, Barlow DP, Zwart R (2001) The extraneuronal monoamine transporter Slc22a3/Orct3 co-localizes with the Maoa metabolizing enzyme in mouse placenta. Mech Dev 100:127-130.
66. Verleysdonk S, Hamprecht B, Rapp M, Wellard J (2004) Uptake and metabolism of serotonin by ependymal primary cultures. Neurochem Res 29:1739-1747.
67. Vermes I, Telegdy G (1972) Effect of intraventricular injection and intrahypothalamic implantation of serotonin on the hypothalamo-hypophyseal- adrenal system in the rat. Acta Physiol Acad Sci Hung 42:49-59.
68. Vermes I, Telegdy G (1973) Effect of 5-hydroxytryptamine on stress-induced adrenal function in the guinea pig. Acta Physiol Acad Sci Hung 43:99-103.
69. Vertes RP, Fortin WJ, Crane AM (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407:555-582.
70. Vialou V, Amphoux A, Zwart R, Giros B, Gautron S (2004) Organic cation transporter 3 (Slc22a3) is implicated in salt-intake regulation. J Neurosci 24:2846-2851.
71. Volk C, Gorboulev V, Budiman T, Nagel G, Koepsell H (2003) Different affinities of inhibitors to the outwardly and inwardly directed substrate binding site of organic cation transporter 2. Mol Pharmacol 64:1037-1047.
72. Watt MJ, Scholl JL, Feng N, Mo B, Forster GL, Lowry CA, Renner KJ (2005) Synergistic effects of corticosterone and progesterone on serotonin levels in the dorsomedial hypothalamus. Soc Neurosci Abstr 31:186.10.
73. Wu X, Kekuda R, Huang W, Fei YJ, Leibach FH, Chen J, Conway SJ, Ganapathy V (1998) Identity of the organic cation transporter OCT3 as the extraneuronal monoamine transporter (uptake2) and evidence for the expression of the transporter in the brain. J Biol Chem 273:32776-32786.