Skip to main content
SpringerLink
Log in

Changes in Ribosomal Protein S3 Immunoreactivity and its Protein Levels in the Gerbil Hippocampus Following Subacute and Chronic Restraint Stress

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Ribosomal protein S3 (rpS3), a multi-functional protein, has been known to participate in DNA repair mechanism. In this study, we investigated changes in rpS3 immunoreactivity and its protein levels in the sub-regions of the gerbil hippocampus following subacute and chronic restraint stress. Serum corticosterone levels were increased in both the subacute and chronic-stress-groups compared to the control-group: the level in the subacute-stress-group was much higher than that in the chronic-stress-group. We could not find any neuronal damage in all the sub-regions of the hippocampus after both the subacute and chronic restraint stress. In the subacute-stress-group, rps3 immunoreactivity was not different compared to the control-group. However, rps3 immunoreactivity in the chronic-stress-group was decreased compared to the subacute-stress-group: especially, the immunoreactivity was markedly decreased in the pyramidal cells of the hippocampus proper (CA1–CA3 region) and granule cells of the dentate gyrus. In addition, western blot analysis also showed that rpS3 protein levels in the chronic-stress-group were significantly decreased compared to those in the subacute-stress-group. These findings indicate that chronic stress, not subacute stress, can decrease rpS3 immunoreactivity.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105–122

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  3. Sapolsky RM (1996) Why stress is bad for your brain. Science 273:749–750

    Article  PubMed  CAS  Google Scholar 

  4. Song L, Zheng J, Li H et al (2009) Prenatal stress causes oxidative damage to mitochondrial DNA in hippocampus of offspring rats. Neurochem Res 34:739–745

    Article  PubMed  CAS  Google Scholar 

  5. Tagliari B, Tagliari AP, Schmitz F et al (2011) Chronic variable stress alters inflammatory and cholinergic parameters in hippocampus of rats. Neurochem Res 36:487–493

    Article  PubMed  CAS  Google Scholar 

  6. Uno H, Tarara R, Else JG et al (1989) Hippocampal damage associated with prolonged and fatal stress in primates. J Neurosci 9:1705–1711

    PubMed  CAS  Google Scholar 

  7. McIntosh LJ, Sapolsky RM (1996) Glucocorticoids increase the accumulation of reactive oxygen species and enhance adriamycin-induced toxicity in neuronal culture. Exp Neurol 141:201–206

    Article  PubMed  CAS  Google Scholar 

  8. Cochrane CG (1991) Mechanisms of oxidant injury of cells. Mol Aspects Med 12:137–147

    Article  PubMed  CAS  Google Scholar 

  9. Kyng KJ, Bohr VA (2005) Gene expression and DNA repair in progeroid syndromes and human aging. Ageing Res Rev 4:579–602

    Article  PubMed  CAS  Google Scholar 

  10. Pham K, Nacher J, Hof PR et al (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 17:879–886

    Article  PubMed  Google Scholar 

  11. Vyas A, Mitra R, Shankaranarayana Rao BS et al (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810–6818

    PubMed  CAS  Google Scholar 

  12. Consiglio AR, Ramos AL, Henriques JA et al (2010) DNA brain damage after stress in rats. Prog Neuropsychopharmacol Biol Psychiatry 34:652–656

    Article  PubMed  CAS  Google Scholar 

  13. Sosnovskii AS, Kozlov AV (1992) Increased lipid peroxidation in the rat hypothalamus after short-term emotional stress. Biull Eksp Biol Med 113:486–488

    Article  PubMed  CAS  Google Scholar 

  14. Jang CY, Lee JY, Kim J (2004) RpS3, a DNA repair endonuclease and ribosomal protein, is involved in apoptosis. FEBS Lett 560:81–85

    Article  PubMed  CAS  Google Scholar 

  15. Kim J, Chubatsu LS, Admon A et al (1995) Implication of mammalian ribosomal protein S3 in the processing of DNA damage. J Biol Chem 270:13620–13629

    Article  PubMed  CAS  Google Scholar 

  16. Kim SH, Kim J (2006) Reduction of invasion in human fibrosarcoma cells by ribosomal protein S3 in conjunction with Nm23-H1 and ERK. Biochim Biophys Acta 1763:823–832

    Article  PubMed  CAS  Google Scholar 

  17. Wilson DM 3rd, Deutsch WA, Kelley MR (1993) Cloning of the Drosophila ribosomal protein S3: another multifunctional ribosomal protein with AP endonuclease DNA repair activity. Nucleic Acids Res 21:2516

    Article  PubMed  CAS  Google Scholar 

  18. Hwang IK, Yoo KY, Kim DW et al (2008) Ischemia-induced ribosomal protein S3 expressional changes and the neuroprotective effect against experimental cerebral ischemic damage. J Neurosci Res 86:1823–1835

    Article  PubMed  CAS  Google Scholar 

  19. Park JH, Yoo KY, Lee CH et al (2011) Comparison of glucocorticoid receptor and ionized calcium-binding adapter molecule 1 immunoreactivity in the adult and aged gerbil hippocampus following repeated restraint stress. Neurochem Res 36:1037–1045

    Article  PubMed  CAS  Google Scholar 

  20. Choi SH, Kim SY, An JJ et al (2006) Immunohistochemical studies of human ribosomal protein S3 (rpS3). J Biochem Mol Biol 39:208–215

    Article  PubMed  CAS  Google Scholar 

  21. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123–130

    Article  PubMed  CAS  Google Scholar 

  22. Yu JT, Lee CH, Yoo KY et al (2010) Maintenance of anti-inflammatory cytokines and reduction of glial activation in the ischemic hippocampal CA1 region preconditioned with lipopolysaccharide. J Neurol Sci 296:69–78

    Article  PubMed  CAS  Google Scholar 

  23. Feldman S, Conforti N (1980) Participation of the dorsal hippocampus in the glucocorticoid feedback effect on adrenocortical activity. Neuroendocrinology 30:52–55

    Article  PubMed  CAS  Google Scholar 

  24. Herman JP, Schafer MK, Young EA et al (1989) Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis. J Neurosci 9:3072–3082

    PubMed  CAS  Google Scholar 

  25. Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453–462

    Article  PubMed  CAS  Google Scholar 

  26. Sapolsky RM, Krey LC, McEwen BS (1985) Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci 5:1222–1227

    PubMed  CAS  Google Scholar 

  27. Madrigal JL, Caso JR, de Cristobal J et al (2003) Effect of subacute and chronic immobilisation stress on the outcome of permanent focal cerebral ischaemia in rats. Brain Res 979:137–145

    Article  PubMed  CAS  Google Scholar 

  28. Lee YJ, Choi B, Lee EH et al (2006) Immobilization stress induces cell death through production of reactive oxygen species in the mouse cerebral cortex. Neurosci Lett 392:27–31

    Article  PubMed  CAS  Google Scholar 

  29. Fontella FU, Siqueira IR, Vasconcellos AP et al (2005) Repeated restraint stress induces oxidative damage in rat hippocampus. Neurochem Res 30:105–111

    Article  PubMed  CAS  Google Scholar 

  30. Muqbil I, Azmi AS, Banu N (2006) Prior exposure to restraint stress enhances 7,12-dimethylbenz(a)anthracene (DMBA) induced DNA damage in rats. FEBS Lett 580:3995–3999

    Article  PubMed  CAS  Google Scholar 

  31. Sapolsky RM, Krey LC, McEwen BS (1986) The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr Rev 7:284–301

    Article  PubMed  CAS  Google Scholar 

  32. Sousa N, Madeira MD, Paula-Barbosa MM (1998) Effects of corticosterone treatment and rehabilitation on the hippocampal formation of neonatal and adult rats. An unbiased stereological study. Brain Res 794:199–210

    Article  PubMed  CAS  Google Scholar 

  33. Benkovic SA, O’Callaghan JP, Miller DB (2009) Protracted exposure to supraphysiological levels of corticosterone does not cause neuronal loss or damage and protects against kainic acid-induced neurotoxicity in the hippocampus of C57BL/6 J mice. Neurotoxicology 30:965–976

    Article  PubMed  CAS  Google Scholar 

  34. Kim BS, Kim MY, Leem YH (2011) Hippocampal neuronal death induced by kainic acid and restraint stress is suppressed by exercise. Neuroscience 194:291–301

    Article  PubMed  CAS  Google Scholar 

  35. Kim SH, Lee JY, Kim J (2005) Characterization of a wide range base-damage-endonuclease activity of mammalian rpS3. Biochem Biophys Res Commun 328:962–967

    Article  PubMed  CAS  Google Scholar 

  36. Lee CH, Yoo KY, Choi JH et al (2011) Ribosomal protein s3 immunoreactivity in the young, adult and aged gerbil hippocampus. J Vet Med Sci 73:361–365

    Article  PubMed  CAS  Google Scholar 

  37. Lee HC, Chang DE, Yeom M et al (2005) Gene expression profiling in hypothalamus of immobilization-stressed mouse using cDNA microarray. Brain Res Mol Brain Res 135:293–300

    Article  PubMed  CAS  Google Scholar 

  38. Fontella FU, Cimarosti H, Crema LM et al (2005) Acute and repeated restraint stress influences cellular damage in rat hippocampal slices exposed to oxygen and glucose deprivation. Brain Res Bull 65:443–450

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Mr. Seung Uk Lee for their technical help in this study. This work was supported by 2011 Research Grant from Kangwon National University, and by Mid-career Researcher Program from the NRF Grant funded by the MEST (2009-0086319).

Author information

Authors and Affiliations

  1. Department of Neurobiology, Institute of Medical Sciences, School of Medicine, Kangwon National University, Chuncheon, 200-701, South Korea

    Joon Ha Park, Bing Chun Yan & Moo-Ho Won

  2. Department of Anatomy and Physiology, College of Pharmacy, Dankook University, Cheonan, 330-714, South Korea

    Choong Hyun Lee

  3. Laboratory of Neuroscience, Department of Physical Therapy, College of Rehabilitation Science, Daegu University, Daegu, 712-714, South Korea

    Ji Hyeon Ahn

  4. Department of Emergency Medicine, Seoul Hospital, College of Medicine, Sooncheonhyang University, Seoul, 140-743, South Korea

    Young Joo Lee

  5. Department of Emergency Medicine, Institute of Medical Sciences, School of Medicine, Kangwon National University Hospital, Kangwon National University, Chuncheon, 200-701, South Korea

    Chan Woo Park & Jun Hwi Cho

  6. Department of Biomedical Sciences, Research Institute for Bioscience and Biotechnology, Hallym University, Chuncheon, 200-702, South Korea

    Soo Young Choi

  7. Department of Physiology, Institute of Neurodegeneration and Neuroregeneration, College of Medicine, Hallym University, Chuncheon, 200-702, South Korea

    Yun Lyul Lee

  8. Department of Internal Medicine, Institute of Medical Sciences, School of Medicine, Kangwon National University, Chuncheon, 200-701, South Korea

    Hui Young Lee

Authors
  1. Joon Ha Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Choong Hyun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bing Chun Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ji Hyeon Ahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Young Joo Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chan Woo Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jun Hwi Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Soo Young Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yun Lyul Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Moo-Ho Won
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hui Young Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Moo-Ho Won or Hui Young Lee.

Additional information

Joon Ha Park and Choong Hyun Lee contributed equally to this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Park, J.H., Lee, C.H., Yan, B.C. et al. Changes in Ribosomal Protein S3 Immunoreactivity and its Protein Levels in the Gerbil Hippocampus Following Subacute and Chronic Restraint Stress. Neurochem Res 37, 1428–1435 (2012). https://doi.org/10.1007/s11064-012-0727-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-012-0727-z

Keywords

Search

Navigation