Polarized expression of the antidepressant-sensitive serotonin transporter in epinephrine-synthesizing chromaffin cells of the rat adrenal gland

Molecular and Cellular Neurosciences

Volumn 9, Issue 3, 1997, Pages 170-184

  Schroeter, Sally ^a   Levey, Allan I ^b   Blakely, Randy D ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; SEROTONIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CHROMAFFIN CELL; CONFOCAL LASER MICROSCOPY; EXTRACELLULAR SPACE; IMMUNOFLUORESCENCE TEST; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS REGULATION; RAT; SEROTONIN UPTAKE;

ANIMALIA; RODENTIA;

EID: 0030849436     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1997.0619     Document Type: Article

References (98)

1. Aguilera G. Factors controlling steroid biosynthesis in the zona glomerulosa of the adrenal. J. Steroid Biochem. Mol. Biol. 45:1993;147-151.
2. Anderson J. M., Stevenson B. R., Jesaitis L. A., Goodenough D. A., Mooseker M. S. Characterization of ZO-1, a protein component of the tight junction from mouse liver and Madin-Darby canine kidney cells. J. Cell Biol. 106:1988;1141-1149.
3. 1A. Trends Neurosci. 19:1996;378-383.
4. Axelrod J. The pineal gland: A neurochemical transducer. Science. 184:1974;1341-1348.
5. ++. Biochim. Biophys. Acta. 719:1982;413-423.
6. Barath P., Csaba G. Effect of pinealectomy on the tritiated serotonin uptake of the adrenal medulla. Horm. Metab. Res. 5:1973;466-470.
7. Blakely R. D., Berson H. E., Fremeau R. T. Jr., Caron M. G., Peek M. M., Prince H. K., Bradley C. C. Molecular cloning and functional expression of a rat brain serotonin transporter. Nature. 354:1991;66-70.
8. Blakely R. D., DeFelice L. J., Hartzell H. C. Molecular physiology of norepinephrine and serotonin transporters. J. Exp. Biol. 196:1994;263-281.
9. Blakely R. D., Moore K. R., Qian Y. Tails of serotonin and norepinephrine transporters: Deletions and chimeras retain function. Molecular Biology and Function of Carrier Proteins. 1993;Rockefeller Univ. Press, New York. p. 283-300.
10. Boess F. G., Martin I. L. Molecular biology of 5-HT receptors. Neuropharmacology. 33:1994;275-317.
11. 125. Synapse. 12:1992;27-36.
12. Bonner-Weir S. Morphological evidence for pancreatic polarity of β-cell within islets of Langerhans. Diabetes. 37:1988;616-621.
13. Brownfield M. S., Poff B. C., Holzwarth M. A. Ultrastructural immunocytochemical co-localization of serotonin and PNMT in adrenal medullary vesicles. Histochemistry. 83:1985;41-46.
14. Carraway R. E., Cochrane D. E., Granier C., Kitabgi P., Leeman E., Singer E. A. Parallel secretion of endogenous 5-hydroxytryptamine and histamine from mast cells stimulated by vasoactive peptides and compound 48/80. Br. J. Pharmacol. 81:1984;227-229.
15. Chang A. S., Chang S. M., Starnes D. M., Schroeter S., Blakely R. D. Molecular cloning and expression of the mouse serotonin transporter. Brain Res. Mol. Brain Res. 43:1996;185-192.
16. Cheatham B., Volchuk A., Kahn C. R., Wang L., Rhodes C. J. Insulin-stimulated translocation of GLUT4 glucose transporters requires SNARE-complex proteins. Proc. Natl. Acad. Sci. USA. 93:1996;15169-15173.
17. 3. J. Pharmacol. Toxicol. Methods. 27:1992;209-216.
18. Ciliax B. J., Heilman C., Demchyshyn L. L., Pristupa Z. B., Ince E., Hersch S. M., Niznik H. B., Levey A. I. The dopamine transporter: Immunochemical characterization and localization in brain. J. Neurosci. 15:1995;1714-1723.
19. 125. Synapse. 12:1992;37-46.
20. Cohen R. A. Interaction of 5-hydroxytryptamine with endothelial cells. Fozard J. R. The Peripheral Actions of 5-Hydroxytryptamine. 1989;182-200 Oxford Univ. Press, New York.
21. Cubells J. F., Kim K. S., Baker H., Volpe B. T., Chung Y., Houpt T. A., Wessel T. C., Joh T. H. Differential in vivo regulation of mRNA encoding the norepinephrine transporter and tyrosine hydroxylase in rat adrenal medulla and locus ceruleus. J. Neurochem. 65:1995;502-509.
22. 33. J. Pharmacol. Exp. Ther. 242:1987;364-371.
23. Dinan T. G. Noradrenergic and serotonergic abnormalities in depression: Stress-induced dysfunction? J. Clin. Psychiatry. 57:1996;14-18.
24. Drubin D. G., Nelson W. J. Origins of cell polarity. Cell. 84:1996;335-344.
25. Eaton S., Simons K. Apical, basal, and lateral cues for epithelial polarization. Cell. 82:1995;5-8.
26. Edwards R. H. The transport of neurotransmitters into synaptic vesicles. Curr. Opin. Neurobiol. 2:1992;586-594.
27. Fernandez-Vivero J., Rodriguez-Sanchez F., Verastegui C., Cordoba Moriano F., Romero A., de Castro J. M. Immunocytochemical distribution of serotonin and neuropeptide Y (NPY) in mouse adrenal gland. Histol. Histopathol. 8:1993;509-520.
28. Freed C., Revay R., Vaughan R. A., Kriek E., Grant S., Uhl G. R., Kuhar M. J. Dopamine transporter immunoreactivity in rat brain. J. Comp. Neurol. 359:1995;340-349.
29. Furman B. L., Waton N. G. 5-Hydroxytryptamine and peripheral secretory mechanisms. Fozard J. R. The Peripheral Actions of 5-Hydroxytryptamine. 1989;274-300 Oxford Univ. Press, New York.
30. Gaisano H. Y., Ghai M., Malkus P. N., Sheu L., Bouquillon A., Bennett M. K., Trimble W. S. Distinct cellular locations of the syntaxin family of proteins in rat pancreatic acinar cells. Mol. Biol. Cell. 7:1996;2019-2027.
31. Gershon M. D., Dreyfus C. F., Pickel V. M., Joh T. H., Reis D. J. Serotonergic neurons in the peripheral nervous system: Identification in gut by immunohistochemical localization of tryptophan hydroxylase. Proc. Natl. Acad. Sci. USA. 74:1977;3086-3089.
32. Gershon M. D., Ross L. Localization of sites of 5-hydroxytryptamine storage and metabolism by radioautography. J. Physiol. 186:1966;477-492.
33. Gianutsos G., Morrow G., Light S., Sweeney M. J. Dopaminergic properties of nomifensine. Pharm. Biochem. Behav. 17:1982;951-954.
34. Gillis C. N., Pitt B. R. The fate of circulating amines within the pulmonary circulation. Annu. Rev. Physiol. 44:1982;269-281.
35. Gottardi C. J., Caplan M. J. An ion-transporting ATPase encodes multiple apical localization signals. J. Cell Biol. 121:1993;283-293.
36. Gu H. H., Ahn J., Caplan M. J., Blakely R. D., Levey A. I., Rudnick G. Cell-specific sorting of biogenic amine transporters expressed in epithelial cells. J. Biol. Chem. 271:1996;18100-18106.
37. Gumbiner B., Simons K. A functional assay for proteins involved in establishing an epithelial occluding barrier: Identification of a uvomorulin-like polypeptide. J. Cell Biol. 102:1986;457-468.
38. 2+. FEBS Lett. 372:1995;39-43.
39. Haning R., Tait S., Tait J. In vitro. Endocrinology. 87:1970;1147-1167.
40. Hersch S. M., Yi H., Ciliax B. J., Levey A. I. Subcellular localization and molecular topology of the dopamine transporter in the striatum and substantia nigra. J. Comp. Neurol. 1997.
41. Hinson J. P., Vinson G. P., Pudney J., Whitehouse B. J. Adrenal mast cells modulate vascular and secretory responses in the intact adrenal gland of the rat. J. Endocrinol. 121:1989;253-260.
42. Hoffman B. J., Mezey E., Brownstein M. J. Cloning of a serotonin transporter affected by antidepressants. Science. 254:1991;579-580.
43. Holman G. D., Cushman S. W. Subcellular localization and trafficking of the GLUT4 glucose transporter isoform in insulin-responsive cells. BioEssays. 16:1994;753-759.
44. Holzwarth M., Brownfield M. Serotonin coexists with epinephrine in rat adrenal medullary cell. Neuroendocrinology. 41:1985;230-236.
45. Holzwarth M., Sawetawan C., Brownfield M. Serotonin-immunoreactivity in the adrenal medulla: Distribution and response to pharmacological manipulation. Brain Res. Bull. 13:1984;299-308.
46. Hurtley S. M. Recycling of a secretory granule membrane protein after stimulated secretion. J. Cell Sci. 106:1993;649-656.
47. Hyttel J. Citalopram - Pharmacological profile of a specific serotonin uptake inhibitor with antidepressant activity. Prog. Neuropsychopharmacol. Biol. Psychiatry. 6:1982;277-295.
48. Idres S., Delarue C., Lefebvre H., Larcher A., Feuilloley M., Vaudry H. Mechanism of action of serotonin on frog adrenal cortex. J. Steroid Biochem. 34:1989;547-550.
49. Ikonen E., Tagaya M., Ullrich O., Montecucco C., Simons K. Different requirements for NSF, SNAP, and Rab proteins in apical and basolateral transport in MDCK cells. Cell. 81:1995;571-580.
50. Jacobs B., Azmitia E. C. Structure and function of the brain serotonin system. Physiol. Rev. 72:1992;165-229.
51. Jacobsson G., Bean A. J., Scheller R. H., Juntti-Berggren L., Deeney J. T., Berggren P.-O., Meister B. Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc. Natl. Acad. Sci. USA. 91:1994;12487-12491.
52. Kannan R., Grant N. J., Aunis D., Langley K. SNAP-25 is differentially expressed by noradrenergic and adrenergic chromaffin cells. FEBS Lett. 385:1996;159-164.
53. Kent C., Coupland R. E. On the uptake and storage of 5-hydroxytryptamine, 5-hydroxytryptophan and catecholamines by adrenal chromaffin cells and nerve endings. Cell. Tissue Res. 236:1984;189-195.
54. Kim K. S., Wessel T. C., Stone D. M., Carver C. H., Joh T. H., Park D. H. Molecular cloning and characterization of cDNA encoding tryptophan hydroxylase from rat central serotonergic neurons. Brain Res. Mol. Brain Res. 9:1991;277-283.
55. Kobayashi S., Coupland R. E. Morphological aspects of chromaffin tissue: The differential fixation of adrenaline and noradrenaline. J. Anat. 183:1993;223-235.
56. 4. Neuroscience. 47:1992;999-1007.
57. Legay C., Faudon M., Hery F., Ternaux J. P. 5-HT metabolism in the intestinal wall of the rat. I. The mucosa. Neurochem. Int. 5:1983;721-727.
58. Lesch K. P., Bengel D., Heils A., Sabol S. Z., Greenberg B. D., Petri S., Benjamin J., Muller C. R., Hamer D. H., Murphy D. L. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science. 274:1996;1527-1531.
59. Levey A. I., Armstrong D. B., Atweh S. F., Terry R. D., Wainer B. H. Monoclonal antibodies to choline acetyltransferase: Production, specificity, and immunohistochemistry. J. Neurosci. 3:1983;1-9.
60. Lidov H. G. W., Grzanna R., Molliver M. E. The serotonin innervation of the cerebral cortex in the rat - An immunohistochemical analysis. Neuroscience. 5:1980;207-227.
61. Lidow M. S., Goldman-Rakic P. S., Gallager D. W., Rakic P. Quantitative autoradiographic mapping of serotonin 5-HT1 and 5-HT2 receptors and uptake sites in the neocortex of the rhesus monkey. J. Comp. Neurol. 280:1989;27-42.
62. Lorang D., Amara S. G., Simerly R. B. Cell-type specific expression of catecholamine transporters in the rat brain. J. Neurosci. 14:1993;4903-4914.
63. Low S.-H., Chapin S. J., Weimbs T., Kömüves L. G., Bennett M. K., Mostov K. E. Differential localization of syntaxin isoforms in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell. 7:1996;2007-2018.
64. 3. J. Neurochem. 59:1992;1856-1861.
65. Melikian H. E., McDonald J. K., Gu H., Rudnick G., Moore K. R., Blakely R. D. Human norepinephrine transporter: Biosynthetic studies using a site-directed polyclonal antibody. J. Biol. Chem. 269:1994;12290-12297.
66. 3. Naunyn-Schmiedeberg's Arch. Pharmacol. 346:1992;203-207.
67. Nirenberg M. J., Vaughan R. A., Uhl G. R., Kuhar M. J., Pickel V. M. The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. J. Neurosci. 16:1996;436-447.
68. Ojakian G. K., Schwimmer R. The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells. J. Cell Biol. 107:1988;2377-2387.
69. Pacholczyk T., Blakely R. D., Amara S. G. Expression cloning of a cocaine- and antidepressant-sensitive human noradrenaline transporter. Nature. 350:1991;350-354.
70. Pfeffer S. R. Transport vesicle docking: SNAREs and associates. Annu. Rev. Cell Dev. Biol. 12:1996;441-461.
71. Pietrini G., Matteoli M., Banker G., Caplan M. J. Isoforms of the Na,K-ATPase are present in both axons and dendrites of hippocampal neurons in culture. Proc. Natl. Acad. Sci. USA. 89:1992;8414-8418.
72. Qian Y., Melikian H. E., Rye D. B., Levey A. I., Blakely R. D. Identification and characterization of antidepressant-sensitive serotonin transporter proteins using site-specific antibodies. J. Neurosci. 1261:1995;1261-1274.
73. Quick M. W., Corey J. L., Davidson N., Lester H. A. Second messengers, trafficking-related proteins, and amino acid residues that contribute to the functional regulation of the rat brain GABA transporter GAT1. J. Neurosci. 17:1997;2967-2979.
74. Racke K., Muscholl E. Uptake of [3H]dopamine into dopaminergic and noradrenergic neurones of the isolated neurointermediate lobe of the rat hypophysis. Effects of desipramine and nomifensine. J. Neurochem. 41:1983;1488-1491.
75. Rapport M. M., Green A. A., Page I. H. Serum vasoconstrictor (serotonin) i.v. isolation and characterisation. J. Biol. Chem. 176:1948;1243.
76. Rodriguez-Boulan E., Powell S. K. Polarity of epithelial and neuronal cells. Annu. Rev. Cell Biol. 8:1992;395-427.
77. Role L. W., Perlman R. L. Catecholamine uptake into isolated adrenal chromaffin cells: Inhibition of uptake by acetylcholine. Neuroscience. 10:1993;987-996.
78. Roth D., Burgoyne R. D. SNAP-25 is present in a SNARE complex in adrenal chromaffin cells. FEBS Lett. 351:1994;207-210.
79. Schroeter S., Blakely R. D. Drug targets in the embryo: Studies on the cocaine and antidepressant-sensitive serotonin transporter. Ann. N.Y. Acad. Sci. 801:1996;239-255.
80. Schubert D., LaCorbiere M., Klier F. G., Steinbach J. H. The modulation of neurotransmitter synthesis by steroid hormones and insulin. Brain Res. 190:1980;67-79.
81. Schwob J. E., Huard J. M., Luskin M. B., Youngentob S. L. Retroviral lineage studies of the rat olfactory epithelium. Chem. Senses. 19:1994;671-682.
82. Shimoyama Y., Hirohashi S., Hirano S., Noguchi M., Shimosato Y., Takeichi M., Abe O. Cadherin cell-adhesion molecules in human epithelial tissues and carcinomas. Cancer Res. 49:1989;2128-2133.
83. 125. J. Pharmacol. Exp. Ther. 273:1995;213-222.
84. Skalli O., Ropraz P., Trzeciak A., Benzonana G., Gillessen D., Gabbiani G. A monoclonal antibody against alpha-smooth muscle actin: A new probe for smooth muscle differentiation. J. Cell Biol. 103:1986;2787-2796.
85. Stoltz J. F. Uptake and storage of serotonin by platelets. Vanhoutte P. M. Serotonin and the Cardiovascular System. 1985;37-42 Raven Press, New York.
86. Suzuki T., Kachi T. Differences between adrenaline and noradrenaline cells in cellular association with supporting cells in the adrenal medulla of the pig: An immunohistochemical study. Neurosci. Lett. 176:1994;217-220.
87. Söllner T., Bennett M. K., Whiteheart S. W., Scheller R. H., Rothman J. E. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation and fusion. Cell. 75:1993;409-418.
88. 14. J. Pharmacol. Exp. Ther. 169:1969;68-73.
89. Trost B. N., Muller J. Uptake and metabolism of serotonin by rat adrenal tissue in vitro. Acta Endocrinol. 82:1976;353-365.
90. Ubink R., Lange R., Verhofstad A. Simultaneous immunoenzymatic staining of catecholamines, catecholamine-biosynthesizing enzymes, and bromodeoxyuridine in adrenal medullary cells of the rat. J. Histochem. Cytochem. 43:1995;39-46.
91. Vandenbergh D. J., Mori N., Anderson D. J. Co-expression of multiple neurotransmitter enzyme genes in normal and immortalized sympathoadrenal progenitor cells. Dev. Biol. 148:1991;10-22.
92. Verhofstad A. A. J., Jonsson G. Immunohistochemical and neurochemical evidence for the presence of serotonin in the adrenal medulla of the rat. Neuroscience. 10:1983;1443-1453.
93. Vijayaraghavan S., Schmid H., Mapp K. S. Serotonin modulates nicotinic responses of adrenal chromaffin cells. J. Neurochem. 61:1993;324-331.
94. Wakade A. R., Wakade T. D., Poosch M., Bannon M. J. Noradrenaline transport and transporter mRNA of rat chromaffin cells are controlled by dexamethasone and nerve growth factor. J. Physiol. 494:1996;67-75.
95. 125125. Mol. Pharmacol. 43:1993;264-270.
96. 2. J. Pharmacol. Exp. Ther. 270:1994;918-928.
97. Wessel T., Joh T. Parallel upregulation of catecholamine-synthesizing enzymes in rat brain and adrenal gland: Effects of reserpine and correlation with immediate early gene expression. Brain Res. Mol. Brain Res. 15:1992;349-360.
98. Yoffe J. R., Borchardt R. Characterization of serotonin uptake in cultured pheochromocytoma cells: Comparison with norepinephrine uptake. Mol. Pharmacol. 21:1982;368-373.