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The hypophysis controls expression of SNAP-25 and other SNAREs in the adrenal gland

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Journal of Neurocytology

Abstract

SNAP-25 (Synaptosomal Associated Protein of 25 kDa), in association with two other SNARE (soluble NSF attachment protein receptor) proteins, syntaxin and Vesicle Associated Membrane Protein, VAMP, is implicated in regulated and constitutive exocytosis in neurones and neuroendocrine cells. Our previous studies have shown that it is expressed more by noradrenergic than adrenergic chromaffin cells in the rat adrenal gland. Since certain hormones under hypophyseal control play an essential role in determining chromaffin cell phenotype, the present study examined the effect of hypophysectomy on SNAP-25 expression. Hypophysectomy was found by immunoblotting and RT-PCR analysis to increase adrenal gland SNAP-25, syntaxin-1 and VAMP-2 levels, without modifying the relative expression of SNAP-25 isoforms: immunocytochemistry showed a dramatic increase in SNAP-25 expression in former adrenergic chromaffin cells. Since adrenal glucocorticoids are considerably reduced by hypophysectomy, the effect of corticosterone replacement therapy was investigated. This did not change levels of SNAP-25, syntaxin-1 or VAMP-2. SNARE expression was also unmodified in pheochromocytoma cells treated with a synthetic glucocorticoid. In contrast, subcutaneous injection of hypophysectomized rats with thyroid hormone decreased adrenal SNAP-25, demonstrating the potential importance of the pituitary-thyroid axis. The current data thus demonstrate that the hypophysis exerts an inhibitory control on adrenal gland SNARE proteins. They suggest that glucocorticoids are unlikely to be directly responsible for this but provide evidence that thyroid hormones are implicated in this phenomenon. The putative role of hormonal regulation on SNARE function is discussed.

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References

  • Boschert, U., O'Shaughnessy, C., Dickinson, R., Tessari, M., Bendotti, C., Catsicas, S. & Pich, E. M. (1996) Developmental and plasticityrelated differential expression of two SNAP-25 isoforms in the rat brain. Journal of Comparative Neurology 367, 177–193.

    Google Scholar 

  • Brunger, A. T. (2000) Structural insights into the molecular mechanism of Ca2+-dependant exocytosis. Current Opinions in Neurobiology 10, 293–302.

    Google Scholar 

  • Ceccatelli, S., Dagerlind, A., Schalling, M., Wikstrom, A. C., Okret, S., Gustafsson, J. A., Goldstein, M. & Hokfelt, T. (1989) The glucocorticoid receptor in the adrenal gland is localized in the cytoplasm of adrenaline cells. Acta Physiologica Scandinavia 137, 559–560.

    Google Scholar 

  • Choi, A. Y., Fukui, H. & Perlman, R. L. (1995) Glucocorticoids enhance histamine-evoked catecholamine secretion from bovine chromaffin cells. Journal of Neurochemistry 64, 206–212.

    Google Scholar 

  • Coupland, R. E., Tomlinson, A., Crowe, J. & Brindley, D. N. (1984) Effects of hypophysectomy and metyrapone on the catecholamine content and volumes of adrenaline-and noradrenaline-storing cells in the rat adrenal medulla. Journal of Endocrinology 101, 345–352.

    Google Scholar 

  • Deans, Z. C., Dawson, S. J., Kilimann, M. W., Wallace, D., Wilson, M. C. & Latchman, D. S. (1997) Differential regulation of genes encoding synaptic proteins by the Oct-2 transcription factor. Molecular Brain Research 51, 1–7.

    Google Scholar 

  • Doupe, A. J., Landis, S. C. & Patterson, P. H. (1985) Environmental influences in the development of neural crest derivatives: Glucocorticoids, growth factors, and chromaffin cell plasticity. Journal of Neuroscience 5, 2119–2142.

    Google Scholar 

  • Ebert, S. N., Balt, S. L., Hunter, J. P., Gashler, A., Sukhatme, V. & Wong, D. L. (1994) Egr1 activation of rat adrenal phenylethanolamine N-methyltransferase gene. Journal of Biological Chemistry 269, 20885–20898.

    Google Scholar 

  • Finotto, S., Krieglstein, K., Schober, A., Deimling, F., Lindner, K., Bruhl, B., Beier, K., Metz, J., Garcia-Arraras, J. E., Roig-Lopez, J. L., Monaghan, P., Schmid, W., Cole, T. J., Kellendonk, C., Tronche, F., Schutz, G. & Unsicker, K. (1999) Analysis of mice carrying targeted mutations of the glucocorticoid receptor gene argues against an essential role of glucocorticoid signalling for generating adrenal chromaffin cells. Development 126, 2935–2944.

    Google Scholar 

  • Grant, N. J., Claudepierre, T., Aunis, D. & Langley, K. (1996) Glucocorticoids and nerve growth factor differentially modulate cell adhesion molecule L1 expression in PC12 cells. Journal of Neurochemistry 66, 1400–1408.

    Google Scholar 

  • Grosse, G., Grosse, J., Tapp, R., Kuchinke, J., Gorsleben, M., Fetter, I., Hohne-Zell, B., Gratzl, M. & Bergmann, M. (1999) SNAP-25 requirement for dendritic growth of hippocampal neurons. Journal of Neuroscience Research 56, 539–546.

    Google Scholar 

  • Grosse, J., Bulling, A., Brucker, C., Berg, U., Amsterdam, A., Mayerhofer, A. & Gratzl, M. (2000) Synaptosome-associated protein of 25 kilodaltons in oocytes and steroid-producing cells of rat and human ovary: Molecular analysis and regulation by gonadotropins. Biology of Reproduction 63, 643–650.

    Google Scholar 

  • Grothe, C., Hofmann, H. D., Verhofstad, A. A. & Unsicker, K. (1985) Nerve growth factor and dexamethasone specify the catecholaminergic phenotype of cultured rat chromaffin cells: Dependence on developmental stage. Brain Research 353, 125–132.

    Google Scholar 

  • Hepp, R., Grant, N. J., Aunis, D. & Langley, K. (2000) SNAP-25 regulation during adrenal gland development: Comparison with differentiation markers and other SNAREs. Journal of Comparative Neurology 421, 533–542.

    Google Scholar 

  • Hepp, R., Grant, N. J., Espliguero, G., Aunis, D., SarliÈve, L. L., Rodriguez-Pena, A. & Langley, K. (2001) Adrenal gland SNAP-25 expression is altered in thyroid hormone receptor knock-out mice. NeuroReport 12, 1427–1430.

    Google Scholar 

  • Hepp, R. & Langley, K. (2001) SNAREs during development. Cell and Tissue Research 305, 247–253.

    Google Scholar 

  • Hofmann, H. D., Seidl, K. & Unsicker, K. (1989) Development and plasticity of adrenal chromaffin cells: Cues based on in vitro studies. Journal of Electron Microscope Techniques 12, 397–407.

    Google Scholar 

  • Jacobsson, G., Razani, H., Ogren, S. O. & Meister, B. (1998) Estrogen down-regulates mRNA encoding the exocytotic protein SNAP-25 in the rat pituitary gland. Journal of Neuroendocrinology 10, 157–163.

    Google Scholar 

  • Jiang, W., Uht, R. & Bohn, M. C. (1989) Regulation of phenylethanolamine N-methyltransferase (PNMT) mRNAin the rat adrenal medulla by corticosterone. International Journal of Developmental Neuroscience 7, 513–520.

    Google Scholar 

  • Kannan, R., Grant, N. J., Aunis, D. & Langley, K. (1996) SNAP-25 is differentially expressed by noradrenergic and adrenergic chromaffin cells. FEBS Letters 385, 159–164.

    Google Scholar 

  • Kelner, K. L. & Pollard, H. B. (1985) Glucocorticoid receptors and regulation of phenylethanolamine-N-methyltransferase activity in cultured chromaffin cells. Journal of Neuroscience 5, 2161–2168.

    Google Scholar 

  • Koibuchi, N. & Chinn, W. W. (2000) Thyroid hormone action on brain development. Trends in Endocrinology and Metabolism 11, 123–128.

    Google Scholar 

  • Lakin, N. D., Morris, P. J., Theil, T., Sato, T. N., Moroy, T., Wilson, M. C. & Latchman, D. S. (1995) Regulation of neurite outgrowth and SNAP-25 gene expression by the Brn-3a transcription factor. Journal of Biological Chemistry 270, 15858–15863.

    Google Scholar 

  • Lee, M. S., Zhu, Y. L., Sun, Z., Rhee, H., Jeromin, A., Roder, J. & Dannies, P. S. (2000) Accumulation of synaptosomal-associated protein of 25 kDa (SNAP-25) and other proteins associated with the secretory pathway in GH4C1 cells upon treatment with estradiol, insulin, and epidermal growth factor. Endocrinology 141, 3485–3492.

    Google Scholar 

  • McKay, L. I. & Cidlowski, J. A. (1999) Molecular control of immune/inflammatory responses: Interactions between nuclear factor-kappa B and steroid receptorsignaling pathways. Endocrinology Reviews 20, 435–459.

    Google Scholar 

  • Meyer, J. S., Micco, D. J., Stephenson, B. S., Krey, L. C. & McEwen, B. S. (1979) Subcutaneous implantation method for chronic glucocorticoid replacement therapy. Physiology of Behavior 22, 867–870.

    Google Scholar 

  • Nawata, H., Yanase, T., Higuchi, K., Kato, K. & Ibayashi, H. (1985) Epinephrine and norepinephrine syntheses are regulated by a glucocorticoid receptormediated mechanism in the bovine adrenal medulla. Life Sciences 36, 1957–1966.

    Google Scholar 

  • Osen-Sand, A., Catsicas, M., Jones, K. A., Ayala, G., Knowles, J., Grenningloh, G. & Catsicas, S. (1993) Inhibition of axonal growth by SNAP-25 antisense oligonucleotides in vitro and in vivo. Nature 364, 445–448.

    Google Scholar 

  • Osen-Sand, A., Staple, J. K., Naldi, E., Schiavo, G., Rossetto, O., Petitpierre, S., Malgaroli, A., Montecucco, C. & Catsicas, S. (1996) Common and distinct fusion proteins in axonal growth and transmitter release. Journal of Comparative Neurology 367, 222–234.

    Google Scholar 

  • Oyler, G. A., Higgins, G. A., Hart, R. A., Battenberg, E., Billingsley, M., Bloom, F. E. & Wilson, M. C. (1989) The identification of a novel synaptosomal-asociated protein, SNAP-25, differentially expressed by neuronal subpopulations. Journal of Cell Biology 109, 3039–3052.

    Google Scholar 

  • Patanow, C. M., Day, J. R. & Billingsley, M. L. (1997) Alterations in hippocampal expression of SNAP-25, GAP-43, stannin and glial fibrillary acidic protein following mechanical and trimethyltin-induced injury in the rat. Neuroscience 76, 187–202.

    Google Scholar 

  • Rothman, J. E. (1994) Mechanisms of intracellular protein transport. Nature 372, 55–63.

    Google Scholar 

  • Sarlieve, L. L., Bouchon, R., Koehl, C. & Neskovic, N. M. (1983) Cerebroside and sulfatide biosynthesis in the brain of Snell dwarf mouse: Effects of thyroxine and growth hormone in the early postnatal period. Journal of Neurochemistry 40, 1058–1062.

    Google Scholar 

  • Seidl, K. & Unsicker, K. (1989) The determination of the adrenal medullary cell fate during embryogenesis. Developmental Biology 136, 481–490.

    Google Scholar 

  • Simonetta, G., Young, I. R. & McMillen, I. C. (1996) Thyroxine replacement after hypophysectomy alters the pattern of enkephalin localisation in the adrenal medulla of the fetal sheep. Journal of the Autonomic Nervous System 59, 60–65.

    Google Scholar 

  • Sollner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. & Rothman, J. E. (1993a) A protein assembly-disassembly pathway in vitro thatmaycorrespond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409–418.

    Google Scholar 

  • Sollner, T. & Rothman, J. E. (1994) Neurotransmission: Harnessing fusion machinery at the synapse. Trends in Neuroscience 17, 344–348.

    Google Scholar 

  • Sollner, T., Whiteheart, S. W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P. & Rothman, J. E. (1993b) SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318–324.

    Google Scholar 

  • Soriano, E., del Rio, J. A., Martinez, A. & Super, H. (1994) Organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical characterization of neuronal populations in the subplate and marginal zone. Journal of Comparative Neurology 342, 571–595.

    Google Scholar 

  • Sudhof, T. C., de Camilli, P., Niemann, H. & Jahn, R. (1993) Membrane fusion machinery: Insights from synaptic proteins. Cell 75, 1–4.

    Google Scholar 

  • Unsicker, K., Finotto, S. & Krieglstein, K. (1997) Generation of cell diversity in the peripheral autonomic nervous system: The sympathoadrenal cell lineage revisited. Annals of Anatomy 179, 495–500.

    Google Scholar 

  • Unsicker, K., Krisch, B., Otten, U. & Theonen, H. (1978) Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: Impairment by glucocorticoids. Proceedings of the National Academy of Science USA 75, 3498–3502.

    Google Scholar 

  • Wan, D. C. & Livett, B. G. (1989) Induction of phenylethanolamine N-methyltransferase mRNA expression by glucocorticoids in cultured bovine adrenal chromaffin cells. European Journal of Pharmacology 172, 107–115.

    Google Scholar 

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Authors
  1. Régine Hepp
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  2. Nancy J. Grant
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  3. Sylvette Chasserot-Golaz
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  4. Dominique Aunis
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  5. Keith Langley
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Hepp, R., Grant, N.J., Chasserot-Golaz, S. et al. The hypophysis controls expression of SNAP-25 and other SNAREs in the adrenal gland. J Neurocytol 30, 789–800 (2001). https://doi.org/10.1023/A:1019689320869

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