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Crowding stress inhibits serotonin 1A receptor-mediated increases in corticotropin-releasing factor mRNA expression and adrenocorticotropin hormone secretion in the Gulf toadfish

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Abstract

Stimulation of the serotonin 1A (5-HT1A) receptor subtype by 5-HT has been shown to result in an elevation in plasma corticosteroid levels in both mammals and several species of teleost fish, including the Gulf toadfish (Opsanus beta); however, in the case of teleost fish, it is not clearly known at which level of the hypothalamic–pituitary–interrenal axis the 5-HT1A receptor is stimulated. Additionally, previous investigations have revealed that chronic elevations of plasma cortisol mediate changes in brain 5-HT1A receptor mRNA and protein levels via the glucocorticoid receptor (GR); thus, we hypothesized that the function of centrally activated 5-HT1A receptors is reduced or abolished as a result of chronically elevated plasma cortisol levels and that this response is GR mediated. Our results are the first to demonstrate that intravenous injection of the 5-HT1A receptor agonist, 8-OH-DPAT, stimulates a significant increase in corticotropin-releasing factor (CRF) precursor mRNA expression in the hypothalamic region and the release of adrenocorticotropic hormone (ACTH) from the pituitary of teleost fish compared to saline-injected controls. We also provide evidence that cortisol, acting via GRs, attenuates the 5-HT1A receptor-mediated secretion of both CRF and ACTH.

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References

  • Alderman SL, Bernier NJ (2007) Localization of corticotropin-releasing factor, urotensin I, and CRF-binding protein gene expression in the brain of the zebrafish, Danio rerio. J Comp Neurol 502(5):783–793. doi:10.1002/cne.21332

    Article  CAS  PubMed  Google Scholar 

  • Arai M, Assil IQ, Abou-Samra AB (2001) Characterization of three corticotropin-releasing factor receptors in catfish: a novel third receptor is predominantly expressed in pituitary and urophysis. Endocrinology 142(1):446–454

    CAS  PubMed  Google Scholar 

  • Backstrom T, Schjolden J, Overli O, Thornqvist PO, Winberg S (2011) Stress effects on AVT and CRF systems in two strains of rainbow trout (Oncorhynchus mykiss) divergent in stress responsiveness. Horm Behav 59(1):180–186. doi:10.1016/j.yhbeh.2010.11.008

    Article  PubMed  Google Scholar 

  • Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38(8):1083–1152

    Article  CAS  PubMed  Google Scholar 

  • Beer M, Kennett GA, Curzon G (1990) A single dose of 8-OH-DPAT reduces raphe binding of [3H]8-OH-DPAT and increases the effect of raphe stimulation on 5-HT metabolism. Eur J Pharmacol 178(2):179–187

    Article  CAS  PubMed  Google Scholar 

  • Bernier NJ (2006) The corticotropin-releasing factor system as a mediator of the appetite-suppressing effects of stress in fish. Gen Comp Endocrinol 146(1):45–55. doi:10.1016/j.ygcen.2005.11.016

    Article  CAS  PubMed  Google Scholar 

  • Bernier NJ, Lin X, Peter RE (1999) Differential expression of corticotropin-releasing factor (CRF) and urotensin I precursor genes, and evidence of CRF gene expression regulated by cortisol in goldfish brain. Gen Comp Endocrinol 116(3):461–477. doi:10.1006/gcen.1999.7386

    Article  CAS  PubMed  Google Scholar 

  • Bernier NJ, Alderman SL, Bristow EN (2008) Heads or tails? Stressor-specific expression of corticotropin-releasing factor and urotensin I in the preoptic area and caudal neurosecretory system of rainbow trout. J Endocrinol 196(3):637–648. doi:10.1677/JOE-07-0568

    Article  CAS  PubMed  Google Scholar 

  • Blier P, de Montigny C (1987) Modification of 5-HT neuron properties by sustained administration of the 5-HT1A agonist gepirone: electrophysiological studies in the rat brain. Synapse 1(5):470–480. doi:10.1002/syn.890010511

    Article  CAS  PubMed  Google Scholar 

  • Bovetto S, Rouillard C, Richard D (1996) Role of CRH in the effects of 5-HT-receptor agonists on food intake and metabolic rate. Am J Physiol 271(5 Pt 2):R1231–R1238

    CAS  PubMed  Google Scholar 

  • Bradford CS, Fitzpatrick MS, Schreck CB (1992) Evidence for ultra-short-loop feedback in ACTH-induced interrenal steroidogenesis in coho salmon: acute self-suppression of cortisol secretion in vitro. Gen Comp Endocrinol 87(2):292–299

    Article  CAS  PubMed  Google Scholar 

  • Calogero AE, Bernardini R, Margioris AN, Bagdy G, Gallucci WT, Munson PJ, Tamarkin L, Tomai TP, Brady L, Gold PW et al (1989) Effects of serotonergic agonists and antagonists on corticotropin-releasing hormone secretion by explanted rat hypothalami. Peptides 10(1):189–200

    Article  CAS  PubMed  Google Scholar 

  • Chang CL, Hsu SY (2004) Ancient evolution of stress-regulating peptides in vertebrates. Peptides 25(10):1681–1688. doi:10.1016/j.peptides.2004.05.022

    Article  CAS  PubMed  Google Scholar 

  • Chaouloff F (1993) Physiopharmacological interactions between stress hormones and central serotonergic systems. Brain Res Brain Res Rev 18(1):1–32

    Article  CAS  PubMed  Google Scholar 

  • Chen CC, Fernald RD (2008) Sequences, expression patterns and regulation of the corticotropin-releasing factor system in a teleost. Gen Comp Endocrinol 157(2):148–155. doi:10.1016/j.ygcen.2008.04.003

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Craig PM, Al-Timimi H, Bernier NJ (2005) Differential increase in forebrain and caudal neurosecretory system corticotropin-releasing factor and urotensin I gene expression associated with seawater transfer in rainbow trout. Endocrinology 146(9):3851–3860

    Article  CAS  PubMed  Google Scholar 

  • Dinan TG (1996) Serotonin and the regulation of hypothalamic–pituitary–adrenal axis function. Life Sci 58(20):1683–1694

    Article  CAS  PubMed  Google Scholar 

  • Fanelli RJ, McMonagle-Strucko K (1992) Alteration of 5-HT1A receptor binding sites following chronic treatment with ipsapirone measured by quantitative autoradiography. Synapse 12(1):75–81. doi:10.1002/syn.890120109

    Article  CAS  PubMed  Google Scholar 

  • Flik G, Klaren PH, Van den Burg EH, Metz JR, Huising MO (2006) CRF and stress in fish. Gen Comp Endocrinol 146(1):36–44. doi:10.1016/j.ygcen.2005.11.005

    Article  CAS  PubMed  Google Scholar 

  • Forlano PM, Marchaterre M, Deitcher DL, Bass AH (2010) Distribution of androgen receptor mRNA expression in vocal, auditory, and neuroendocrine circuits in a teleost fish. J Comp Neurol 518(4):493–512. doi:10.1002/cne.22233

    Google Scholar 

  • Fryer JN, Peter RE (1977) Hypothalamic control of ACTH secretion in goldfish. III. Hypothalamic cortisol implant studies. Gen Comp Endocrinol 33(2):215–225

    Article  CAS  PubMed  Google Scholar 

  • Fryer J, Lederis K, Rivier J (1984) Cortisol inhibits the ACTH-releasing activity of urotensin I, CRF and sauvagine observed with superfused goldfish pituitary cells. Peptides 5(5):925–930

    Article  CAS  PubMed  Google Scholar 

  • Fuller RW (1990) Serotonin receptors and neuroendocrine responses. Neuropsychopharmacology 3(5–6):495–502

    CAS  PubMed  Google Scholar 

  • Fuzzen ML, Van Der Kraak G, Bernier NJ (2010) Stirring up new ideas about the regulation of the hypothalamic–pituitary–interrenal axis in zebrafish (Danio rerio). Zebrafish 7(4):349–358. doi:10.1089/zeb.2010.0662

    Article  CAS  PubMed  Google Scholar 

  • Gobbi M, Cavanus S, Miari A, Mennini T (1991) Effect of acute and chronic administration of buspirone on serotonin and benzodiazepine receptor subtypes in the rat brain: an autoradiographic study. Neuropharmacology 30(4):313–321

    Article  CAS  PubMed  Google Scholar 

  • Grosell M, Mager EM, Williams C, Taylor JR (2009) High rates of HCO3 secretion and Cl absorption against adverse gradients in the marine teleost intestine: the involvement of an electrogenic anion exchanger and H+-pump metabolon? J Exp Biol 212(Pt 11):1684–1696. doi:10.1242/jeb.027730

    Article  CAS  PubMed  Google Scholar 

  • Höglund E, Balm PH, Winberg S (2002) Stimulatory and inhibitory effects of 5-HT(1A) receptors on adrenocorticotropic hormone and cortisol secretion in a teleost fish, the Arctic charr (Salvelinus alpinus). Neurosci Lett 324(3):193–196

    Article  PubMed  Google Scholar 

  • Jørgensen H, Knigge U, Kjaer A, Moller M, Warberg J (2002) Serotonergic stimulation of corticotropin-releasing hormone and pro-opiomelanocortin gene expression. J Neuroendocrinol 14(10):788–795

    Article  PubMed  Google Scholar 

  • Kageyama K, Tozawa F, Horiba N, Watanobe H, Suda T (1998) Serotonin stimulates corticotropin-releasing factor gene expression in the hypothalamic paraventricular nucleus of conscious rats. Neurosci Lett 243(1–3):17–20

    Article  CAS  PubMed  Google Scholar 

  • Kasckow JW, Regmi A, Gill PS, Parkes DG, Geracioti TD (1997) Regulation of corticotropin-releasing factor (CRF) messenger ribonucleic acid and CRF peptide in the amygdala: studies in primary amygdalar cultures. Endocrinology 138(11):4774–4782

    Article  CAS  PubMed  Google Scholar 

  • Kennett GA, Marcou M, Dourish CT, Curzon G (1987) Single administration of 5-HT1A agonists decreases 5-HT1A presynaptic, but not postsynaptic receptor-mediated responses: relationship to antidepressant-like action. Eur J Pharmacol 138(1):53–60

    Article  CAS  PubMed  Google Scholar 

  • Lastein S, Höglund E, Overli O, Doving KB (2008) Effects of antalarmin, a CRF receptor 1 antagonist, on fright reaction and endocrine stress response in crucian carp (Carassius carassius). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 194(12):1007–1012. doi:10.1007/s00359-008-0372-9

    Article  CAS  PubMed  Google Scholar 

  • Lim JE, Porteus CS, Bernier NJ (2013) Serotonin directly stimulates cortisol secretion from the interrenals in goldfish. Gen Comp Endocrinol 192:246–255. doi:10.1016/j.ygcen.2013.08.008

    Article  CAS  PubMed  Google Scholar 

  • Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC(T) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Martinez JA, Bueno L (1991) Buspirone inhibits corticotropin-releasing factor and stress-induced cecal motor response in rats by acting through 5-HT1A receptors. Eur J Pharmacol 202(3):379–383

    Article  CAS  PubMed  Google Scholar 

  • Mauk MD, Peroutka SJ, Kocsis JD (1988) Buspirone attenuates synaptic activation of hippocampal pyramidal cells. J Neurosci 8(1):1–11

    CAS  PubMed  Google Scholar 

  • McDonald MD, Walsh PJ (2004) Dogmas and controversies in the handling of nitrogenous wastes: 5-HT2-like receptors are involved in triggering pulsatile urea excretion in the gulf toadfish, Opsanus beta. J Exp Biol 207(Pt 12):2003–2010

    Article  CAS  PubMed  Google Scholar 

  • McDonald MD, Wood CM, Wang Y, Walsh PJ (2000) Differential branchial and renal handling of urea, acetamide and thiourea in the gulf toadfish Opsanus beta: evidence for two transporters. J Exp Biol 203(Pt 6):1027–1037

    CAS  PubMed  Google Scholar 

  • McDonald MD, Wood CM, Grosell M, Walsh PJ (2004) Glucocorticoid receptors are involved in the regulation of pulsatile urea excretion in toadfish. J Comp Physiol [B] 174(8):649–658. doi:10.1007/s00360-004-0456-y

    Article  CAS  Google Scholar 

  • McDonald MD, Vulesevic B, Perry SF, Walsh PJ (2009) Urea transporter and glutamine synthetase regulation and localization in gulf toadfish gill. J Exp Biol 212(Pt 5):704–712. doi:10.1242/jeb.015875

    Article  CAS  PubMed  Google Scholar 

  • Medeiros LR, McDonald MD (2012) Elevated cortisol inhibits adrenocorticotropic hormone- and serotonin-stimulated cortisol secretion from the interrenal cells of the Gulf toadfish (Opsanus beta). Gen Comp Endocrinol 179(3):414–420. doi:10.1016/j.ygcen.2012.09.011

    Article  CAS  PubMed  Google Scholar 

  • Medeiros LR, McDonald MD (2013) Cortisol-mediated downregulation of the serotonin 1A receptor subtype in the Gulf toadfish, Opsanus beta. Comp Biochem Physiol A Mol Integr Physiol 164(4):612–621. doi:10.1016/j.cbpa.2013.01.014

    Article  CAS  PubMed  Google Scholar 

  • Medeiros LR, Mager EM, Grosell M, McDonald MD (2010) The serotonin subtype 1A receptor regulates cortisol secretion in the Gulf toadfish, Opsanus beta. Gen Comp Endocrinol 168(3):377–387

    Article  CAS  PubMed  Google Scholar 

  • Nieuwenhuys R, Donkelaar HJT, Nicholson C (1998) The central nervous system of vertebrates. Springer, New York

    Book  Google Scholar 

  • Parent A (1981) Comparative anatomy of the serotonergic systems. J Physiol (Paris) 77:147–156

    CAS  Google Scholar 

  • Parent A, Poitras D, Dubé L (1984) Comparative anatomy of the central monoaminergic systems. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy. Elsevier, Amsterdam, pp 409–439

    Google Scholar 

  • Peroutka SJ, Howell T (1997) 5-Hydroxytryptamine receptors. In: Bittar EE, Bittar N (eds) Molecular and cellular pharmacology. Principles of medical biology, vol 8. Elsevier, Amsterdam, pp 59–72

  • Polter AM, Li X (2010) 5-HT1A receptor-regulated signal transduction pathways in brain. Cell Signal 22(10):1406–1412. doi:10.1016/j.cellsig.2010.03.019

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rodela TM, McDonald MD, Walsh PJ, Gilmour KM (2009) The regulatory role of glucocorticoid and mineralocorticoid receptors in pulsatile urea excretion of the gulf toadfish, Opsanus beta. J Exp Biol 212(Pt 12):1849–1858. doi:10.1242/jeb.026997

    Article  CAS  PubMed  Google Scholar 

  • Schechter LE, Bolanos FJ, Gozlan H, Lanfumey L, Haj-Dahmane S, Laporte AM, Fattacini CM, Hamon M (1990) Alterations of central serotonergic and dopaminergic neurotransmitters in rats chronically treated with ipsapirone: biochemical and electrophysiological studies. J Pharmacol Exp Ther 255:1335–1347

    CAS  PubMed  Google Scholar 

  • Simpson ER, Waterman MR (1988) Regulation of the synthesis of steroidogenic enzymes in adrenal cortical cells by ACTH. Annu Rev Physiol 50:427–440. doi:10.1146/annurev.ph.50.030188.002235

    Article  CAS  PubMed  Google Scholar 

  • Sloman KA, McDonald MD, Barimo JF, Lepage O, Winberg S, Wood CM, Walsh PJ (2005) Does pulsatile urea excretion serve as a social signal in the gulf toadfish Opsanus beta? Physiol Biochem Zool 78(5):724–735

    Article  CAS  PubMed  Google Scholar 

  • Sprouse JS, Aghajanian GK (1987) Electrophysiological responses of serotoninergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse 1(1):3–9. doi:10.1002/syn.890010103

    Article  CAS  PubMed  Google Scholar 

  • Sprouse JS, Aghajanian GK (1988) Responses of hippocampal pyramidal cells to putative serotonin 5-HT1A and 5-HT1B agonists: a comparative study with dorsal raphe neurons. Neuropharmacology 27(7):707–715

    Article  CAS  PubMed  Google Scholar 

  • Stoskopf M (1993) Fish medicine. W.B. Saunders Co., Philadelphia

    Google Scholar 

  • Sullivan NR, Crane JW, Damjanoska KJ, Carrasco GA, D’Souza DN, Garcia F, Van de Kar LD (2005) Tandospirone activates neuroendocrine and ERK (MAP kinase) signaling pathways specifically through 5-HT1A receptor mechanisms in vivo. Naunyn Schmiedebergs Arch Pharmacol 371(1):18–26. doi:10.1007/s00210-004-1005-7

    Article  CAS  PubMed  Google Scholar 

  • Tsigos C, Chrousos GP (2002) Hypothalamic–pituitary–adrenal axis, neuroendocrine factors and stress. J Psychosom Res 53(4):865–871

    Article  PubMed  Google Scholar 

  • Van de Kar LD, Lorens SA, Urban JH, Bethea CL (1989) Effect of selective serotonin (5-HT) agonists and 5-HT2 antagonist on prolactin secretion. Neuropharmacology 28:299–305

    Article  PubMed  Google Scholar 

  • Wang LH, Tsai CL (2006) Influence of temperature and gonadal steroids on the ontogenetic expression of brain serotonin 1A and 1D receptors during the critical period of sexual differentiation in tilapia, Oreochromis mossambicus. Comp Biochem Physiol B Biochem Mol Biol 143(1):116–125. doi:10.1016/j.cbpb.2005.10.010

    Article  PubMed  Google Scholar 

  • Wang HT, Han F, Shi YX (2009) Activity of the 5-HT1A receptor is involved in the alteration of glucocorticoid receptor in hippocampus and corticotropin-releasing factor in hypothalamus in SPS rats. Int J Mol Med 24(2):227–231

    CAS  PubMed  Google Scholar 

  • Welch JE, Farrar GE, Dunn AJ, Saphier D (1993) Central 5-HT1A receptors inhibit adrenocortical secretion. Neuroendocrinology 57(2):272–281

    Article  CAS  PubMed  Google Scholar 

  • Willenberg HS, Bornstein SR, Hiroi N, Path G, Goretzki PE, Scherbaum WA, Chrousos GP (2000) Effects of a novel corticotropin-releasing-hormone receptor type I antagonist on human adrenal function. Mol Psychiatry 5(2):137–141

    Article  CAS  PubMed  Google Scholar 

  • Winberg S, Nilsson G (1996) Multiple high-affinity binding sites for [3H]serotonin in the brain of a teleost fish, the Arctic charr (Salvelinus alpinus). J Exp Biol 199(Pt 11):2429–2435

    CAS  PubMed  Google Scholar 

  • Winberg S, Nilsson A, Hylland P, Soderstom V, Nilsson GE (1997) Serotonin as a regulator of hypothalamic–pituitary–interrenal activity in teleost fish. Neurosci Lett 230(2):113–116

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi F, Brenner S (1997) Molecular cloning of 5-hydroxytryptamine (5-HT) type 1 receptor genes from the Japanese puffer fish, Fugu rubripes. Gene 191(2):219–223

    Article  CAS  PubMed  Google Scholar 

  • Young G (1993) Effects of hypophysectomy on coho salmon interrenal: maintenance of steroidogenic pathway and restoration of in vitro responsiveness to adrenocorticotropin after handling. Gen Comp Endocrinol 92(3):428–438. doi:10.1006/gcen.1993.1179

    Article  CAS  PubMed  Google Scholar 

  • Zifa E, Fillion G (1992) 5-Hydroxytryptamine receptors. Pharmacol Rev 44(3):401–458

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Mr. Ray Hurley and Ms. Debbie Fretz for providing toadfish for the experiments conducted herein, the NSF Grant IOS-0920547 (to M. Danielle McDonald) as well as the Rowlands fellowship and the Knight Fellowship to Lea R. Medeiros.

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The authors are not aware of any conflicts of interest, financial or otherwise.

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Correspondence to Lea R. Medeiros.

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Communicated by H.V. Carey.

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Medeiros, L.R., Cartolano, M.C. & McDonald, M.D. Crowding stress inhibits serotonin 1A receptor-mediated increases in corticotropin-releasing factor mRNA expression and adrenocorticotropin hormone secretion in the Gulf toadfish. J Comp Physiol B 184, 259–271 (2014). https://doi.org/10.1007/s00360-013-0793-9

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