Abstract
Stress causes endocrinological changes and leads to induce anxiety. It was determined the anxiety and stress-related endocrinological changes through the observation of the level of glucocorticoid and sphingolipid metabolites in serum after stress. Immobilized stress and electric shock was applied to rats for 7 days. This study investigated the induction of anxiety, changes of TH and pERK expression in cortex and amygdala after stress. Also it was determined the changes of glucocorticoid and anxiety when the rats were given stress after amygdala lesion. The stress-given rats spent a lesser percentage of time significantly in the open arm than the control rats. The elevated level of glucocorticoid after stress was suppressed in amygdala lesion group. The expression of TH in the amygdala was decreased, but the expression of TH was not changed in the cortex after stress. To investigate the changes in sphingolipid metabolites after stress, the levels of sphingosine and the phosphate form of sphingolipid (So-1-P) were analyzed in serum. The level of So-1-P was elevated after stress and anxiety was observed after the So-1-P infusion (100 pmol/10 μl/h, i.c.v., for 7 days). Continuous infusion of So-1-P for 7 days led to the significant decrease of TH expression in the amygdala. In conclusion, the results of this study indicate that the lesion of amygdala suppressed the stress-induced anxiety and elevation of glucocorticoid in serum. It was also observed that expression of TH in amygdala as well as increased levels of glucocorticoid in serum might be responsible biomarker, at least in part, of chronic stress. These results suggest that the elevation of So-1-P might be involved in induction of anxiety during stress by the modulation of dopaminergic system in amygdala.
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References
McEwen BS (2000) The neurobiology of stress: from serendipity to clinical relevance. Brain Res 886:172–189
Selye H (1936) A syndrome produced by diverse noxious agents. Nature 138:32
Kim CS, Jo YJ, Park SH, Kim HJ, Han JY, Hong JT, Cheong JH, Oh KW (2010) Anti-stress effects of ginsenoside Rg3-standardized ginseng extract in restraint stressed animals. Biomol Ther 18:219–225
Nankova B, Kvetnansky R, Hiremagalur B, Sabban B, Rusnak M, Sabban EL (1996) Immobilization stress elevates gene expression for catecholamine biosynthetic enzymes and some neuropeptides in rat sympathetic ganglia: effects of adrenocorticotropin and glucocorticoids. Endocrinology 137:5597–5604
Chida Y, Sudo N, Sonoda J, Sogawa H, Kubo C (2004) Electric foot shock stress-induced exacerbation of alpha-galactosylceramide-triggered apoptosis in mouse liver. Hepatology 39:1131–1140
Baria O, Sibel A, Arslan FB (2004) Influence of surgical pain stress on the blood-brain barrier permeability in rats. Life Sci 74:1973–1979
Katouli M, Bark T, Ljungqvist O, Svenberg T, Möllby R (1994) Composition and diversity of intestinal coliform flora influence bacterial translocation in rats after hemorrhagic stress. Infect Immun 62:4768–4774
Feng Q, Cheng B, Yang R, Sun FY, Zhu CQ (2005) Dynamic changes of phosphorylated tau in mouse hippocampus after cold water stress. Neurosci Lett 388:13–16
Azusa IS, Asuka MO, Ohata H, Naoko Y, Tamotsu S (2009) Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological stress in rats. Psychoneuroendocrinology 34:226–237
Van de Kar LD, Piechowski RA, Rittenhouse PA, Gray TS (1991) Amygdaloid lesions: differential effect on conditioned stress and immobilization-induced increases in corticosterone and renin secretion. Neuroendocrinology 54:89–95
Hogg S (1996) A review of the validity and variability of the Elevated Plus-Maze as an animal model of anxiety. Pharmacol Biochem Behav 54:21–30
Gregus A, Wintink AJ, Davis AC, Kalynchuk LE (2005) Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav Brain Res 156:105–114
Maryam AM, Alredro C, Mohammed K (2000) Repeated immobilization stress increases total cytosolic glucocorticoid receptor in rat liver. Steroids 65:8–15
Zhao Y, Ma R, Shen J, Su H, Xing D (2008) A mouse model of depression induced by repeated corticosterone injections. Eur J Pharmacol 581:113–120
Gewirtz GP, Weise VK, Kopin IJ (1970) Effect of hypophysectomy on immobilization-induced elevation of tyrosine hydroxylase and phenylethanolamine-N-methyl transferase in the rat adrenal. Endocrinology 87:1323–1329
Masserano JM, Takimoto GS, Weiner N (1981) Electroconvulsive shock increases tyrosine hydroxylase activity in the brain and adrenal gland of the rat. Science 214:662–665
Gilad GM, McCarty R (1981) Differences in choline acetyltransferase but similarities in catecholamine biosynthetic enzymes in brains of two rat strains differing in their response to stress. Brain Res 206:239–243
Shen CP, Tsimberg Y, Salvadore C, Meller E (2004) Activation of Erk and JNK MAPK pathways by acute swim stress in rat brain regions. BMC Neurosci 5:1–13
Wu SL, Hsu LS, Tu WT, Wang WF, Huang YT, Pawlak CR (2008) Effects of d-cycloserine on the behavior and ERK activity in the amygdala: role of individual anxiety levels. Behav Brain Res 187:246–253
Gourley SL, Wu FJ, Kiraly DD, Ploski JE, Kedves AT, Duman RS, Taylor JR (2008) Regionally specific regulation of ERK MAP Kinase in a model of antidepressant-sensitive chronic depression. Biol Psychiatry 63:353–359
Hisaoka K, Nishida A, Koda T, Miyata M, Zensho H, Morinobu A (2001) Antidepressant drug treatments induce glial cell line-derived neurotrophic factor (GDNF) synthesis and release in rat C6 glioblastoma cells. J Neurochem 2001:25–34
Tiraboschi E, Tardito D, Kasahara J, Moraschi S, Pruneri P, Gennarelli M (2004) Selective phosphorylation of nuclear CREB by fluoxetine is linked to activation of CaM kinase IV and MAP kinase cascades. Neuropsychopharmacology 29:1831–1840
Dwivedi Y, Rizavi HS, Conley RR, Pandey GN (2006) ERK MAP kinase signaling in post-mortem brain of suicide subjects: differential regulation of upstream Raf kinases Raf-1 and B-Raf. Mol Psychiatry 11:86–98
Taha TA, Mullen TD, Obeid LM (2006) A house divided: ceramide, sphingosine, and aphingosine-1-phosphate in programmed cell death. Biochim Biophys Acta 1758:2027–2036
Davaille J, Li L, Mallat A, Lotersztajin S (2002) Sphingosine-1-phosphate triggers both apoptotic and survival for human hepatic myofibroblasts. J Biol Chem 277:37323–37330
Jang S, Suh SH, Yoo HS, Lee YM, Oh S (2008) Changes of iNOS, GFAP and NR1 expression in various brain regions and elevation of sphingosine-1-phosphate in serum after immobilized stress. Neurochem Res 33:842–851
Stutzmann GE, LeDoux JE (1999) GABAergic antagonists block the inhibitory effects of serotonin in the lateral amygdala: a mechanism for modulation of sensory inputs related to fear conditioning. J Neurosci 19:1–4
Gallagher M, Chiba AA (1996) The amygdale and emotion. Curr Opin Neurobiol 6:221–227
Musacchio JM, Louis J, Seymour SK, Jacques G (1969) Increase in rat brain tyrosine hydroxylase activity produced by electroconvulsive shock. Proc Natl Acad Sci USA 63:1117–1119
Conrad CD, LeDoux JE, Magarinos AM, McEwen BS (1999) Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 113:902–913
Pardon MC, Gould GG, Garcia A, Phillips L, Cook MC, Miller SA, Mason PA, Morilak DA (2002) Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders. Neuroscience 115:229–242
Parker KJ, Schatzberg AF, Lyons DM (2003) Neuroendocrine aspects of hypercortisolism in major depression. Hormone Behav 43:60–66
Vyas A, Mitra R, Rao BSS, Chattarij S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810–6818
Burns LH, Everitt BJ, Robbins TW (1999) Effects of excitotoxic lesions of the basolateral amygdale on conditional discrimination learning with primary and conditioned reinforcement. Behav Brain Res 100:123–133
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, San Diego 135 pp
Kimura T, Miyaoka T, Saunders PA, Baker ML, Hume AS, Yamamoto I, Ho IK (1993) Induction of tolerance to and physical dependence on pentobarbital continuous intracerebroventricular administration. J Pharmacol Exp Ther 266:1300–1305
Dawson GR, Tricklebank MD (1995) Use of the elevated plus maze in the search for novel anxiolytic agents. Curr Tech 16:84–88
Woodward C, Emery PW (1988) Determination of plasma corticosterone using high-performance liquid chromatography. J Chromatogr 419:280–284
Min JK, Yoo HS, Lee EY, Lee WJ, Lee YM (2002) Simultaneous quantitative analysis of sphingoid base 1-phosphates in biological samples by o-phthalaldehyde precolumn derivatization after dephosphorylation with alkaline phosphatase. Anal Biochem 303:167–175
Yamano Y, Yoshioka M, Toda Y, Oshida Y, Chaki S, Hamamoto K, Morishima I (2004) Regulation of CRF, POMC and MC4R gene expression after electrical foot shock stress in the rat amygdala and hypothalamus. J Vet Med Sci 9:1323–1327
Hatfield T, Han JS, Conley M, Gallagher M, Holland P (1996) Neurotoxic lesions of basolateral, but not central, amygdale interfere with Pavlovian second-order conditioning and reinforcer devaluation effects. J Neurosci 16:5256–5265
Hitchcott PK, Phillips GD (1998) Double dissociation of the behavioural effects of R(+) 7OH-DPAT infusion in the central and basolateral amygdale nuclei upon Pavlovian and instrumental conditioned appetitive behaviours. Psychopharmacology 140:458–469
Watanabe T, Yamamoto R, Maeda A, Nakagawa T, Minami M, Satoh M (2002) Effects of excitotoxic lesions of the central or basolateral nucleus of the amygdale on naloxone-precipitated withdrawal-induced conditioned place aversion in morphine-dependent rats. Brain Res 958:423–428
Qian YR, Kim YS (2007) Effect of immobilization stress on the expression of TH, BDH and CRH gene in rat brain. J Genet Med 4:179–185
Habib KE, Gold PW, Chrousos GP (2001) Neuroendocrinology of stress. Endocrinol Metab Clin North Am 30:695–728
Stratakis CA, Chrouson GP (1995) Neuroendocrinology and pathophysiology of the stress system. Ann NY Acad Sci 771:1–18
Glavin GB (1985) Stress and brain noradrenaline. Neurosci Biobehav Rev 9:233–244
Rastogi RB, Singhal RL (1978) Evidence for the role of adrenocortical hormones in the regulation of noradrenaline and dopamine metabolism in crertain brain areas. Br J Pharmacol 62:131–136
Rabano M, Pena A, Brizuela L, Marino A, Macarulla JM, Trueba M, Gomez-Munoz A (2003) Sphingosine-1-phosphate stimulates cortisol secretion. FEBS Lett 535:101–105
Nayak D, Huo Y, Kwang WXT, Pushparaj PN, Kumar SD, Ling EA, Dheen ST (2010) Sphingosine kinase 1 regulates the expression of proinflammatory cytokines and nitric oxide in activated microglia. Neuroscience 166:132–144
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This work was supported by the Korea Research Foundation Grant funded by the Korean Government (MOEHRD, Basic Research Promotion Fund) (KRF-2007-313-E00627).
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Jang, S., Kim, D., Lee, Y. et al. Modulation of Sphingosine 1-Phosphate and Tyrosine Hydroxylase in the Stress-Induced Anxiety. Neurochem Res 36, 258–267 (2011). https://doi.org/10.1007/s11064-010-0313-1
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DOI: https://doi.org/10.1007/s11064-010-0313-1