Skip to main content

Advertisement

Log in

Modulation of Sphingosine 1-Phosphate and Tyrosine Hydroxylase in the Stress-Induced Anxiety

  • ORIGINAL PAPER
  • Published:
Neurochemical Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. McEwen BS (2000) The neurobiology of stress: from serendipity to clinical relevance. Brain Res 886:172–189

    Article  CAS  PubMed  Google Scholar 

  2. Selye H (1936) A syndrome produced by diverse noxious agents. Nature 138:32

    Article  Google Scholar 

  3. 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

    Article  Google Scholar 

  4. 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

    Article  CAS  PubMed  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  Google Scholar 

  7. 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

    CAS  PubMed  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. 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

    Article  Google Scholar 

  10. 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

    Article  PubMed  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. Maryam AM, Alredro C, Mohammed K (2000) Repeated immobilization stress increases total cytosolic glucocorticoid receptor in rat liver. Steroids 65:8–15

    Article  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. 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

    Article  PubMed  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  CAS  PubMed  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. 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

    Google Scholar 

  22. 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

    Article  CAS  PubMed  Google Scholar 

  23. 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

    Article  CAS  PubMed  Google Scholar 

  24. 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

    Article  CAS  PubMed  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. 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

    Article  CAS  PubMed  Google Scholar 

  27. 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

    Google Scholar 

  28. Gallagher M, Chiba AA (1996) The amygdale and emotion. Curr Opin Neurobiol 6:221–227

    Article  CAS  PubMed  Google Scholar 

  29. 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

    Article  CAS  PubMed  Google Scholar 

  30. 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

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  CAS  PubMed  Google Scholar 

  32. Parker KJ, Schatzberg AF, Lyons DM (2003) Neuroendocrine aspects of hypercortisolism in major depression. Hormone Behav 43:60–66

    Article  CAS  Google Scholar 

  33. 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

    CAS  PubMed  Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, San Diego 135 pp

    Google Scholar 

  36. 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

    CAS  PubMed  Google Scholar 

  37. Dawson GR, Tricklebank MD (1995) Use of the elevated plus maze in the search for novel anxiolytic agents. Curr Tech 16:84–88

    Google Scholar 

  38. Woodward C, Emery PW (1988) Determination of plasma corticosterone using high-performance liquid chromatography. J Chromatogr 419:280–284

    Google Scholar 

  39. 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

    Article  CAS  PubMed  Google Scholar 

  40. 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

    Article  Google Scholar 

  41. 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

    CAS  PubMed  Google Scholar 

  42. 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

    Article  CAS  PubMed  Google Scholar 

  43. 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

    Article  CAS  PubMed  Google Scholar 

  44. 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

    Google Scholar 

  45. Habib KE, Gold PW, Chrousos GP (2001) Neuroendocrinology of stress. Endocrinol Metab Clin North Am 30:695–728

    Article  CAS  PubMed  Google Scholar 

  46. Stratakis CA, Chrouson GP (1995) Neuroendocrinology and pathophysiology of the stress system. Ann NY Acad Sci 771:1–18

    Article  CAS  PubMed  Google Scholar 

  47. Glavin GB (1985) Stress and brain noradrenaline. Neurosci Biobehav Rev 9:233–244

    Article  CAS  PubMed  Google Scholar 

  48. 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

    CAS  PubMed  Google Scholar 

  49. 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

    Article  CAS  PubMed  Google Scholar 

  50. 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Korea Research Foundation Grant funded by the Korean Government (MOEHRD, Basic Research Promotion Fund) (KRF-2007-313-E00627).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seikwan Oh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-010-0313-1

Keywords

Navigation