Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1997 Apr 1;323(Pt 1):251–258. doi: 10.1042/bj3230251

5-Hydroxytryptamine-induced calcium-channel gating in rainbow trout (Oncorhynchus mykiss) peripheral blood lymphocytes.

F Ferriere 1, N A Khan 1, J P Meyniel 1, P Deschaux 1
PMCID: PMC1218303  PMID: 9173890

Abstract

The present study was conducted on peripheral blood lympho-cytes of rainbow trout (Oncorhynchus mykiss) to assess the role of 5-hydroxytryptamine (5-HT; 'serotonin') in calcium signalling. 5-HT-induced increases in intracellular free calcium concentrations, [Ca2+]i, and its action was mediated by 5-HT receptor subtype 3 (5-HT3), but not by 5-HT receptor subtype 1A (5-HT1A) or subtype 2 (5-HT2) in these cells. In Ca2+-containing medium (1 mM CaCl2), 5-HT and 2-methyl-5-HT (5-HT3 receptor agonist) induced increases in [Ca2+]i, whereas in Ca2+-free medium (0 Ca2+, 1 mM EGTA), these two agents failed to evoke increases in [Ca2+]i in these cells, demonstrating that 5-HT mobilizes Ca2+ from the extracellular environment. Furthermore, 5-HT-induced increases in [Ca2+]i are not contributed to by the intracellular endoplasmic reticulum (ER) pool, as thapsigargin, an agent that recruits Ca2+ from ER stores, had additive effects on 5-HT-induced [Ca2+]i responses in fish peripheral lymphocytes. 5-HT-induced increases in [Ca2+]i were mediated by 5-HT3 receptors via gating the calcium through L-type, but not N-type, calcium channels in trout lymphocytes.

Full Text

The Full Text of this article is available as a PDF (455.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aune T. M., Kelley K. A., Ranges G. E., Bombara M. P. Serotonin-activated signal transduction via serotonin receptors on Jurkat cells. J Immunol. 1990 Sep 15;145(6):1826–1831. [PubMed] [Google Scholar]
  2. Aune T. M., McGrath K. M., Sarr T., Bombara M. P., Kelley K. A. Expression of 5HT1a receptors on activated human T cells. Regulation of cyclic AMP levels and T cell proliferation by 5-hydroxytryptamine. J Immunol. 1993 Aug 1;151(3):1175–1183. [PubMed] [Google Scholar]
  3. Besedovsky H. O., del Rey A. E., Sorkin E. Immune-neuroendocrine interactions. J Immunol. 1985 Aug;135(2 Suppl):750s–754s. [PubMed] [Google Scholar]
  4. Bolaños F. J., Schechter L. E., Miquel M. C., Emerit M. B., Rumigny J. F., Hamon M., Gozlan H. Common pharmacological and physico-chemical properties of 5-HT3 binding sites in the rat cerebral cortex and NG 108-15 clonal cells. Biochem Pharmacol. 1990 Oct 1;40(7):1541–1550. doi: 10.1016/0006-2952(90)90452-q. [DOI] [PubMed] [Google Scholar]
  5. Bolliet V., Ali M. A. Immunohistochemical study of the development of serotoninergic neurons in the brain of the brook trout Salvelinus fontinalis. Brain Behav Evol. 1992;40(5):234–249. doi: 10.1159/000113915. [DOI] [PubMed] [Google Scholar]
  6. Codignola A., Tarroni P., Clementi F., Pollo A., Lovallo M., Carbone E., Sher E. Calcium channel subtypes controlling serotonin release from human small cell lung carcinoma cell lines. J Biol Chem. 1993 Dec 15;268(35):26240–26247. [PubMed] [Google Scholar]
  7. Evans D. L., Harris D. T., Jaso-Friedmann L. Function associated molecules on nonspecific cytotoxic cells: role in calcium signaling, redirected lysis, and modulation of cytotoxicity. Dev Comp Immunol. 1992 Sep-Oct;16(5):383–394. doi: 10.1016/0145-305x(92)90040-j. [DOI] [PubMed] [Google Scholar]
  8. Ferriere F., Khan N. A., Troutaud D., Deschaux P. Serotonin modulation of lymphocyte proliferation via 5-HT1A receptors in rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol. 1996 Jul-Aug;20(4):273–283. doi: 10.1016/0145-305x(96)00012-2. [DOI] [PubMed] [Google Scholar]
  9. Fleshner M., Watkins L. R., Lockwood L. L., Bellgrau D., Laudenslager M. L., Maier S. F. Specific changes in lymphocyte subpopulations: a potential mechanism for stress-induced immunomodulation. J Neuroimmunol. 1992 Dec;41(2):131–142. doi: 10.1016/0165-5728(92)90063-q. [DOI] [PubMed] [Google Scholar]
  10. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  11. Hagiwara S., Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. doi: 10.1146/annurev.ne.04.030181.000441. [DOI] [PubMed] [Google Scholar]
  12. Harbuz M. S., Lightman S. L. Stress and the hypothalamo-pituitary-adrenal axis: acute, chronic and immunological activation. J Endocrinol. 1992 Sep;134(3):327–339. doi: 10.1677/joe.0.1340327. [DOI] [PubMed] [Google Scholar]
  13. Hellstrand K., Hermodsson S. Role of serotonin in the regulation of human natural killer cell cytotoxicity. J Immunol. 1987 Aug 1;139(3):869–875. [PubMed] [Google Scholar]
  14. Hesketh T. R., Moore J. P., Morris J. D., Taylor M. V., Rogers J., Smith G. A., Metcalfe J. C. A common sequence of calcium and pH signals in the mitogenic stimulation of eukaryotic cells. Nature. 1985 Feb 7;313(6002):481–484. doi: 10.1038/313481a0. [DOI] [PubMed] [Google Scholar]
  15. Holmqvist B. I., Ekström P. Hypophysiotrophic systems in the brain of the Atlantic salmon. Neuronal innervation of the pituitary and the origin of pituitary dopamine and nonapeptides identified by means of combined carbocyanine tract tracing and immunocytochemistry. J Chem Neuroanat. 1995 Feb;8(2):125–145. doi: 10.1016/0891-0618(94)00041-q. [DOI] [PubMed] [Google Scholar]
  16. Jackson J. C., Cross R. J., Walker R. F., Markesbery W. R., Brooks W. H., Roszman T. L. Influence of serotonin on the immune response. Immunology. 1985 Mar;54(3):505–512. [PMC free article] [PubMed] [Google Scholar]
  17. Janković B. D. Neuroimmunomodulation: facts and dilemmas. Immunol Lett. 1989 May;21(2):101–118. doi: 10.1016/0165-2478(89)90046-1. [DOI] [PubMed] [Google Scholar]
  18. Khan I. A., Bhardwaj G., Malla N., Wattal C., Agarwal S. C. Effect of serotonin on T lymphocyte proliferation in vitro in healthy individuals. Int Arch Allergy Appl Immunol. 1986;81(4):378–380. doi: 10.1159/000234168. [DOI] [PubMed] [Google Scholar]
  19. Khan N. A., Ferriere F., Deschaux P. Serotonin-induced calcium signaling via 5-HT1A receptors in human leukemia (K 562) cells. Cell Immunol. 1995 Oct 1;165(1):148–152. doi: 10.1006/cimm.1995.1198. [DOI] [PubMed] [Google Scholar]
  20. Khan N. A., Kalra V. Urinary 5-HIAA and VMA and their relationship with immunoregulatory cells in stress administered subjects. Arch Immunol Ther Exp (Warsz) 1988;36(6):717–721. [PubMed] [Google Scholar]
  21. Lichtman A. H., Segel G. B., Lichtman M. A. The role of calcium in lymphocyte proliferation. (An interpretive review). Blood. 1983 Mar;61(3):413–422. [PubMed] [Google Scholar]
  22. Liu C., Hermann T. E. Characterization of ionomycin as a calcium ionophore. J Biol Chem. 1978 Sep 10;253(17):5892–5894. [PubMed] [Google Scholar]
  23. Mori Y., Ando M. Regulation of ion and water transport across the eel intestine: effects of acetylcholine and serotonin. J Comp Physiol B. 1991;161(4):387–392. doi: 10.1007/BF00260798. [DOI] [PubMed] [Google Scholar]
  24. Peroutka S. J. 5-Hydroxytryptamine receptors. J Neurochem. 1993 Feb;60(2):408–416. doi: 10.1111/j.1471-4159.1993.tb03166.x. [DOI] [PubMed] [Google Scholar]
  25. Pollock W. K., Sage S. O., Rink T. J. Stimulation of Ca2+ efflux from fura-2-loaded platelets activated by thrombin or phorbol myristate acetate. FEBS Lett. 1987 Jan 5;210(2):132–136. doi: 10.1016/0014-5793(87)81322-4. [DOI] [PubMed] [Google Scholar]
  26. Prpić V., Green K. C., Blackmore P. F., Exton J. H. Vasopressin-, angiotensin II-, and alpha 1-adrenergic-induced inhibition of Ca2+ transport by rat liver plasma membrane vesicles. J Biol Chem. 1984 Feb 10;259(3):1382–1385. [PubMed] [Google Scholar]
  27. Pucilowski O., Kostowski W. Aggressive behaviour and the central serotonergic systems. Behav Brain Res. 1983 Jul;9(1):33–48. doi: 10.1016/0166-4328(83)90012-8. [DOI] [PubMed] [Google Scholar]
  28. Rampe D., Triggle D. J. New ligands for L-type Ca2+ channels. Trends Pharmacol Sci. 1990 Mar;11(3):112–115. doi: 10.1016/0165-6147(90)90196-f. [DOI] [PubMed] [Google Scholar]
  29. Rasmussen H., Kojima I., Kojima K., Zawalich W., Apfeldorf W. Calcium as intracellular messenger: sensitivity modulation, C-kinase pathway, and sustained cellular response. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1984;18:159–193. [PubMed] [Google Scholar]
  30. Reiser G., Donié F., Binmöller F. J. Serotonin regulates cytosolic Ca2+ activity and membrane potential in a neuronal and in a glial cell line via 5-HT3 and 5-HT2 receptors by different mechanisms. J Cell Sci. 1989 Jul;93(Pt 3):545–555. doi: 10.1242/jcs.93.3.545. [DOI] [PubMed] [Google Scholar]
  31. Saligaut C., Salbert G., Bailhache T., Bennani S., Jego P. Serotonin and dopamine turnover in the female rainbow trout (Oncorhynchus mykiss) brain and pituitary: changes during the annual reproductive cycle. Gen Comp Endocrinol. 1992 Feb;85(2):261–268. doi: 10.1016/0016-6480(92)90010-h. [DOI] [PubMed] [Google Scholar]
  32. Sarkar F. H., Singh R. H., Udupa K. N. Effect of electric shock on serotonin (5 HT) content in different organs of rat. Experientia. 1977 Apr 15;33(4):417–418. doi: 10.1007/BF01922185. [DOI] [PubMed] [Google Scholar]
  33. Sternberg E. M., Trial J., Parker C. W. Effect of serotonin on murine macrophages: suppression of Ia expression by serotonin and its reversal by 5-HT2 serotonergic receptor antagonists. J Immunol. 1986 Jul 1;137(1):276–282. [PubMed] [Google Scholar]
  34. Thastrup O., Cullen P. J., Drøbak B. K., Hanley M. R., Dawson A. P. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2466–2470. doi: 10.1073/pnas.87.7.2466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tolloczko B., Jia Y. L., Martin J. G. Serotonin-evoked calcium transients in airway smooth muscle cells. Am J Physiol. 1995 Aug;269(2 Pt 1):L234–L240. doi: 10.1152/ajplung.1995.269.2.L234. [DOI] [PubMed] [Google Scholar]
  36. Tsien R. W. Calcium channels in excitable cell membranes. Annu Rev Physiol. 1983;45:341–358. doi: 10.1146/annurev.ph.45.030183.002013. [DOI] [PubMed] [Google Scholar]
  37. Winberg S., Myrberg A. A., Jr, Nilsson G. E. Predator exposure alters brain serotonin metabolism in bicolour damselfish. Neuroreport. 1993 Apr;4(4):399–402. doi: 10.1097/00001756-199304000-00014. [DOI] [PubMed] [Google Scholar]
  38. Winberg S., Nilsson G. E., Olsén K. H. Changes in brain serotonergic activity during hierarchic behavior in Arctic charr (Salvelinus alpinus L.) are socially induced. J Comp Physiol A. 1992 Jan;170(1):93–99. doi: 10.1007/BF00190404. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES