Stress-specific changes of galanin and PACAP expression in the rat hypothalamus and adrenal gland

Authors

  • Iva Lakić Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, Faculty of Biology University of Belgrade, Studentski trg 16, 11000 Belgrade
  • Tanja Jevđović Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, Faculty of Biology University of Belgrade, Studentski trg 16, 11000 Belgrade
  • Nebojša Jasnić Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, Faculty of Biology University of Belgrade, Studentski trg 16, 11000 Belgrade
  • Tamara Dakić Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, Faculty of Biology University of Belgrade, Studentski trg 16, 11000 Belgrade
  • Predrag Vujović Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, Faculty of Biology University of Belgrade, Studentski trg 16, 11000 Belgrade
  • Jelena Đorđević Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, Faculty of Biology University of Belgrade, Studentski trg 16, 11000 Belgrade

Keywords:

galanin, hypothalamo-pituitary-adrenal (HPA), immobilization, pituitary adenylate cyclase-activating polypeptide (PACAP), restraint, stress

Abstract

Paper dfescription:

  • Neuropeptides galanin and pituitary adenylate cyclase-activating peptide (PACAP) play an important role in mediating the stress response.
  • We showed for the first time that galanin and PACAP displayed specific responses which depended on the duration and type of stressor, with hypothalamic and adrenal expression of galanin and PACAP mRNA increased after repeated restraint and acute immobilization, respectively.
  • Unlike PACAP which remained unchanged, the hypothalamic galanin content increased regardless of the type and duration of applied stressor.
  • Both galanin and PACAP levels remained unaffected by the stressors in the adrenal gland.


Abstract: Galanin and pituitary adenylate cyclase-activating peptide (PACAP) are involved in the stress response, and both produce multiple effects in the central and peripheral nervous systems. In rodents, galanin brain expression is altered by different stressors, while PACAP has a critical role in the circuits mediating the stress-response. The aim of this study was to investigate whether acute and/or repeated immobilization (IMO) and restraint (R) differently affect galanin and PACAP expression in the rat hypothalamus and adrenal gland. Relative expression of mRNAs was examined by qPCR and relative changes in the protein content were analyzed using Western blotting. The distribution of galanin and PACAP peptides in the hypothalamus was analyzed by immunofluorescence. Relative hypothalamic expression of both galanin and PACAP mRNAs was increased only after repeated restraint. Hypothalamic galanin protein levels were increased after all applied stressors, whereas there were no changes in the PACAP content. In the adrenal glands, galanin and PACAP mRNAs were elevated only after acute IMO, whereas the protein levels were not changed, regardless of the applied stressor or its duration. Immunofluorescence staining demonstrated the presence of galanin in the paraventricular nuclei (PVN) of the hypothalamus in all groups. Galanin immunoreactivity was stronger in the PVN of all stressed groups in comparison to the control. We concluded that the patterns of transcriptional activation and translational control of galanin and PACAP in the examined tissues depended on the type (IMO vs. R) and duration (acute vs. repeated) of the applied stressor.

https://doi.org/10.2298/ABS180228008L

Received: February 28, 2018; Revised: March 13, 2018; Accepted: March 13, 2018; Published online: March 21, 2018

How to cite this article: Lakić I, Jevđović T, Jasnić N, Dakić T, Vujović P, Đorđević J. Stress-specific changes of galanin and PACAP expression in the rat hypothalamus and adrenal gland. Arch Biol Sci. 2018;70(3):…

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References

Pacak K, Palkovits M, Kopin IJ, Goldstein DS. Stress-induced norepinephrine release in the hypothalamic paraventricular nucleus and pituitary-adrenocortical and sympathoadrenal activity: in vivo microdialysis studies. Front Neuroendocrinol. 1995;16(2):89-150.

Herman JP, Cullinan WE. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 1997;20(2):78-84.

Bergonzelli GE, Pralong FP, Glauser M, Cavadas C, Grouzmann E, Gaillard RC. Interplay between galanin and leptin in the hypothalamic control of feeding via corticotropin-releasing hormone and neuropeptide Y. Diabetes. 2001;50(12):2666-72.

Malendowicz LK, Nussdorfer GG, Nowak KW, Mazzocchi G. The possible involvement of galanin in the modulation of the function of rat pituitary-adrenocortical axis under basal and stressful conditions. Endocr Res. 1994;20(3):307-17.

Mazzocchi G, Malendowicz LK, Rebuffat P, Nussdorfer GG. Effects of galanin on the secretory activity of the rat adrenal cortex: in vivo and in vitro studies. Res Exp Med (Berl). 1992;192(6):373-81.

Bartfai T, Hokfelt T, Langel U. Galanin--a neuroendocrine peptide. Crit Rev Neurobiol. 1993;7(3-4):229-74.

Sweerts BW, Jarrott B, Lawrence AL. Expression of preprogalanin mRNA following acute and chronic restraint stress in brains of normotensive and hypertensive rats. Brain Res Mol Brain Res. 1999;69(1):113-23.

Ceccatelli S, Eriksson M, Hokfelt T. Distribution and coexistence of corticotropin-releasing factor-, neurotensin-, enkephalin-, cholecystokinin-, galanin- and vasoactive intestinal polypeptide/peptide histidine isoleucine-like peptides in the parvocellular part of the paraventricular nucleus. Neuroendocrinology. 1989;49(3):309-23.

Landry M, Trembleau A, Arai R, Calas A. Evidence for a colocalization of oxytocin mRNA and galanin in magnocellular hypothalamic neurons: a study combining in situ hybridization and immunohistochemistry. Brain Res Mol Brain Res. 1991;10(1):91-5.

Wrenn CC, Holmes A. The role of galanin in modulating stress-related neural pathways. Drug News Perspect. 2006;19(8):461-7.

Andreis PG, Malendowicz LK, Rebuffat P, Spinazzi R, Ziolkowska A, Nussdorfer GG. Galanin enhances corticosterone secretion from dispersed rat adrenocortical cells through the activation of GAL-R1 and GAL-R2 receptors coupled to the adenylate cyclase-dependent signaling cascade. Int J Mol Med. 2007;19(1):149-55.

Ceresini G, Sgoifo A, Freddi M, Musso E, Parmigiani S, Del Rio G, Valenti G. Effects of galanin and the galanin receptor antagonist galantide on plasma catecholamine levels during a psychosocial stress stimulus in rats. Neuroendocrinology. 1998;67(1):67-72.

Miyata A, Arimura A, Dahl RR, Minamino N, Uehara A, Jiang L, Culler MD, Coy DH. Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun. 1989;164(1):567-74.

Hannibal J, Mikkelsen JD, Fahrenkrug J, Larsen PJ. Pituitary adenylate cyclase-activating peptide gene expression in corticotropin-releasing factor-containing parvicellular neurons of the rat hypothalamic paraventricular nucleus is induced by colchicine, but not by adrenalectomy, acute osmotic, ether, or restraint stress. Endocrinology. 1995;136(9):4116-24.

Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, Fournier A, Chow BK, Hashimoto H, Galas L, Vaudry H. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev. 2009;61(3):283-357.

Chiodera P, Volpi R, Capretti L, Caffarri G, Magotti MG, Coiro V. Effects of intravenously infused pituitary adenylate cyclase-activating polypeptide on adenohypophyseal Hormone secretion in normal men. Neuroendocrinology. 1996;64(3):242-6.

Boutillier AL, Monnier D, Koch B, Loeffler JP. Pituitary adenyl cyclase-activating peptide: a hypophysiotropic factor that stimulates proopiomelanocortin gene transcription, and proopiomelanocortin-derived peptide secretion in corticotropic cells. Neuroendocrinology. 1994;60(5):493-502.

Dow RC, Bennie J, Fink G. Pituitary adenylate cyclase-activating peptide-38 (PACAP)-38 is released into hypophysial portal blood in the normal male and female rat. J Endocrinol. 1994;142(1):R1-4.

Hanniba J, Mikkelsen JD, Fahrenkrug J, Larsen PJ. Pituitary adenylate cyclase-activating peptide gene expression in corticotropin-releasing factor-containing parvicellular neurons of the rat hypothalamic paraventricular nucleus is induced by colchicine, but not by adrenalectomy, acute osmotic, ether, or restraint stress. Endocrinology. 1995;136(9):4116-24.

Kvetnansky R, Mikulaj L. Adrenal and urinary catecholamines in rats during adaptation to repeated immobilization stress. Endocrinology. 1970;87(4):738-43.

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402-8.

Lakic I, Vujovic P, Jasnic N, Djurasevic S, Cvijic G. Vasopressin modulates hypothalamo-pituitary activity by paracrine actin during acute and chronic immobilization stress in rats. Arc Biol Sci. 2011;63(3):579-87.

Lachuer J, Delton I, Buda M, Tappaz M. The habituation of brainstem catecholaminergic groups to chronic daily restraint stress is stress specific like that of the hypothalamo-pituitary-adrenal axis. Brain Res. 1994;638(1-2):196-202.

Hannibal J, Jessop DS, Fahrenkrug J, Harbuz MS, Larsen PJ. PACAP gene expression in neurons of the rat hypothalamo-pituitary-adrenocortical axis is induced by endotoxin and interleukin-1beta. Neuroendocrinology. 1999;70(1):73-82.

Holmes A, Picciotto MR. Galanin: a novel therapeutic target for depression, anxiety disorders and drug addiction? CNS Neurol Disord Drug Targets. 2006;5(2):225-232.

Tian Q, Stepaniants SB, Mao M, Weng L, Feetham MC, Doyle MJ, Yi EC, Dai H, Thorsson V, Eng J, Goodlett D, Berger JP, Gunter B, Linseley PS, Stoughton RB, Aebersold R, Collins SJ, Hanlon WA, Hood LE. Integrated genomic and proteomic analyses of gene expression in Mammalian cells. Mol Cell Proteomics. 2004;3(10):960-9.

Vogel C, Marcotte EM. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet. 2012;13(4):227-32.

Gai WP, Geffen LB, Blessing WW. Galanin immunoreactive neurons in the human hypothalamus: colocalization with vasopressin-containing neurons. J Comp Neurol. 1990;298(3):265-80.

Levin MC, Sawchenko PE, Howe PR, Bloom SR, Polak JM. Organization of galanin-immunoreactive inputs to the paraventricular nucleus with special reference to their relationship to catecholaminergic afferents. J Comp Neurol. 1987;261(4):562-82.

Crivellato E, Nico B, Ribatti D. The chromaffin vesicle: advances in understanding the composition of a versatile, multifunctional secretory organelle. Anat Rec (Hoboken). 2008;291(12):1587-602.

Stroth N, Eiden LE. Stress hormone synthesis in mouse hypothalamus and adrenal gland triggered by restraint is dependent on pituitary adenylate cyclase-activating polypeptide signaling. Neuroscience. 2010;165(4):1025-30.

Anouar Y, Eiden LE. Rapid and long-lasting increase in galanin mRNA levels in rat adrenal medulla following insulin-induced reflex splanchnic nerve stimulation. Neuroendocrinology. 1995;62(6):611-8.

Munck A, Guyre PM, Holbrook NJ. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev. 1984;5(1):25-44.

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Published

2018-08-20

How to Cite

1.
Lakić I, Jevđović T, Jasnić N, Dakić T, Vujović P, Đorđević J. Stress-specific changes of galanin and PACAP expression in the rat hypothalamus and adrenal gland. Arch Biol Sci [Internet]. 2018Aug.20 [cited 2024Dec.22];70(3):481-8. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/2638

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Vol. 70 No. 3 (2018)

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