Abstract
Oxidative stress is one of predisposing factors to age-related neurodegeneration in the brain. In particular, thiol-containing groups are susceptible to oxidative stress, which induces the formation of the disulfide bond and/or hyperoxidized form of thiol-containing proteins. We observed the protein thiol levels in the hippocampal homogenates and also investigated changes in hyperoxidized form of peroxiredoxin (Prx–SO3) immunoreactivity and proteins levels in the gerbil hippocampal subregions during normal aging. Levels of total thiol, non-protein thiol, and protein thiol were decreased in the hippocampal homogenates with age. At post-natal month 1 (PM 1), pyramidal and non-pyramidal cells in the hippocampal CA1 region (CA1) showed Prx–SO3 immunoreactivity. Prx–SO3 immunoreactivity in the cells was decreased by PM 12, thereafter, Prx–SO3 immunoreactivity in the cells increased again with age. In the CA2/3, Prx–SO3 immunoreactivity in pyramidal cells was not significantly changed; however, the immunoreactivity in pyramidal cells was very low at PM 12. Prx–SO3 immunoreactivity in the dentate gyrus (DG) was distinctly changed during aging. At PM 1, Prx–SO3 immunoreactivity in granule and polymorphic cells was weak and strong, respectively. The immunoreactivity in the neurons was decreased with age, not shown in any neurons at PM 12. Thereafter, Prx–SO3 immunoreactivity increased again with age. In addition, Prx–SO3 protein level in the hippocampus was lowest at PM 12. These results suggest that thiol-containing proteins are changed during aging and Prx–SO3 immunoreactivity was different according to cells in the hippocampal subregion during aging.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Babusikova E, Hatok J, Dobrota D, Kaplan P (2007) Age-related oxidative modifications of proteins and lipids in rat brain. Neurochem Res 32:1351–1356. doi:10.1007/s11064-007-9314-0
Balu M, Sangeetha P, Murali G, Panneerselvam C (2005) Age-related oxidative damages in central nervous system of rats: modulatory role of grape seed extract. Int J Dev Neurosci 23:501–507. doi:10.1016/j.ijdevneu.2005.06.001
Barnes CA (1994) Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci 17:13–18. doi:10.1016/0166-2236(94)90029-9
Broillet MC (1999) S-nitrosylation of proteins. Cell Mol Life Sci 55:1036–1042. doi:10.1007/s000180050354
Chae HZ, Rhee SG (1994) A thiol-specific antioxidant and sequence homology to various proteins of unknown function. Biofactors 4:177–180
Del Bel EA, Guimarães FS, Bermúdez-Echeverry M, Gomes MZ, Schiaveto-de-souza A, Padovan-Neto FE, Tumas V, Barion-Cavalcanti AP, Lazzarini M, Nucci-da-Silva LP, de Paula-Souza D (2005) Role of nitric oxide on motor behavior. Cell Mol Neurobiol 25:371–392. doi:10.1007/s10571-005-3065-8
Floyd RA, Carney JM (1991) Age influence on oxidative events during brain ischemia/reperfusion. Arch Gerontol Geriatr 12:155–177. doi:10.1016/0167-4943(91)90025-L
Halliwell B, Gutteridge JM (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186:1–85. doi:10.1016/0076-6879(90)86093-B
Iciek M, Chwatko G, Lorenc-Koci E, Bald E, Włodek L (2004) Plasma levels of total, free and protein bound thiols as well as sulfane sulfur in different age groups of rats. Acta Biochim Pol 51:815–824
Khanna P, Nehru B (2007) Antioxidant enzymatic system in neuronal and glial cells enriched fractions of rat brain after aluminum exposure. Cell Mol Neurobiol 27:959–969. doi:10.1007/s10571-007-9233-2
Loskota WA, Lomax P, Verity MA (1974) A stereotaxic atlas of the Mongolian Gerbil Brain (Meriones unguiculatus). Ann Arbor Science Publishers Inc., Ann Arbor, pp 70–79
Mansoor MA, Svardal AM, Schneede J, Ueland PM (1992) Dynamic relation between reduced, oxidized, and protein-bound homocysteine and other thiol components in plasma during methionine loading in healthy men. Clin Chem 38:1316–1321
Rhee SG, Kim KH, Chae HZ, Yim MB, Uchida K, Netto LE, Stadtman ER (1994) Antioxidant defense mechanisms: a new thiol-specific antioxidant enzyme. Ann N Y Acad Sci 738:86–92
Rokutan K, Johnston RB Jr, Kawai K (1994) Oxidative stress induces S-thiolation of specific proteins in cultured gastric mucosal cells. Am J Physiol 266:G247–G254
Samiec PS, Drews-Botsch C, Flagg EW, Kurtz JC, Sternberg P Jr, Reed RL, Jones DP (1998) Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic Biol Med 24:699–704. doi:10.1016/S0891-5849(97)00286-4
Schoneich C (1999) Reactive oxygen species and biological aging: a mechanistic approach. Exp Gerontol 34:19–34. doi:10.1016/S0531-5565(98)00066-7
Sedlak J, Lindsay RH (1968) Estimation of total, protein bound, and non-protein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205. doi:10.1016/0003-2697(68)90092-4
Shacter E (2000) Protein oxidative damage. Methods Enzymol 319:428–436. doi:10.1016/S0076-6879(00)19040-8
Shin CM, Chung YH, Km MJ, Lee EY, Kim EG, Cha CI (2002) Age-related changes in the distribution of nitrotyrosine in the cerebral cortex and hippocampus of rats. Brain Res 931:194–199. doi:10.1016/S0006-8993(01)03391-1
Sies H (1985) Oxidative stress introductory comments. In: Sies H (ed) Oxidative stress. Academic Press, London, pp 1–8
Small SA, Chawla MK, Buonocore M, Rapp PR, Barnes CA (2004) Imaging correlates of brain function in monkeys and rats isolates a hippocampal subregion differentially vulnerable to aging. Proc Natl Acad Sci USA 101:7181–7186. doi:10.1073/pnas.0400285101
Stadtman ER (1992) Protein oxidation and aging. Science 257:1220–1224. doi:10.1126/science.1355616
Stadtman ER, Berlett BS (1997) Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol 10:485–494. doi:10.1021/tx960133r
Stadtman ER, Levine RL (2003) Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25:207–218. doi:10.1007/s00726-003-0011-2
Woo HA, Chae HZ, Hwang SC, Yang KS, Kang SW, Kim K, Rhee SG (2003) Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300:653–656. doi:10.1126/science.1080273
Wood ZA, Schröder E, Robin Harris J, Poole LB (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28:32–40. doi:10.1016/S0968-0004(02)00003-8
Acknowledgments
The authors would like to thank Mr. Suek Han, Seung Uk Lee and Ms. Hyun Sook Kim for their technical help in this study. This work was supported by the MRC program of MOST/KOSEF (R13-2005-022-01002-0).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yoo, KY., Park, O.K., Yu, J. et al. Expression and Changes of Hyperoxidized Peroxiredoxins in Non-Pyramidal and Polymorphic Cells in the Gerbil Hippocampus During Normal Aging. Cell Mol Neurobiol 29, 413–421 (2009). https://doi.org/10.1007/s10571-008-9333-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10571-008-9333-7