Advertisement

Neurochemical Research

, Volume 36, Issue 8, pp 1490–1500 | Cite as

Distribution and Time-Course of 4-Hydroxynonenal, Heat Shock Protein 110/105 Family Members and Cyclooxygenase-2 Expression in the Hippocampus of Rat During Trimethyltin-Induced Neurodegeneration

  • V. Corvino
  • E. Marchese
  • N. Zarkovic
  • K. Zarkovic
  • M. Cindric
  • G. Waeg
  • F. MichettiEmail author
  • M. C. Geloso
Original Paper

Abstract

Trimethyltin (TMT), an organotin compound considered a useful tool to obtain an experimental model of neurodegeneration, exhibits neurotoxicant effects selectively localised in the limbic system and especially in the hippocampus, which are different in the rat and in mice. In the rat hippocampus, we investigated the expression of aldehyde 4-hydroxynonenal, a major bioactive marker of membrane lipid peroxidation, heat shock protein (HSP) 110/105 family members, markers of oxidative stress, and the neuroinflammatory marker cyclooxygenase-2 after TMT-intoxication at various time points after treatment. Our data show that TMT-induced neurodegeneration in the rat hippocampus is associated specifically with oxidative stress and lipid peroxidation, but not with HSP expression, indicating species-specific differences in the neurotoxicity of TMT between rats and mice.

Keywords

Neurodegeneration 4-hydroxynonenal Heat shock proteins COX-2 Trimethyltin Lipid peroxidation 

Notes

Acknowledgments

We would like to thank Prof. N. Miani for useful discussion and Mr D. Bonvissuto and Mr K. Baltazar Del Carmen for excellent technical support. This work was partially supported by funds from Università Cattolica del S. Cuore to F.M, M.C.G. and V.C.

References

  1. 1.
    Coyle JT, Puttfarken P (1993) Oxidative stress, glutamate and neurodegenerative disorders. Science 262:689–695PubMedCrossRefGoogle Scholar
  2. 2.
    Zarkovic N, Zarkovic K, Schaur RJ et al (1999) 4-Hydroxynonenal as a second messenger of free radicals and growth modifying factor. Life Sci 65:1901–1904PubMedCrossRefGoogle Scholar
  3. 3.
    Zarkovic N, Gasparovic AC, Cindric M et al (2009) 4-Hydroxynonenal-protein adducts as biomarkers of oxidative stress, lipid peroxidation and oxidative homeostasis. In: Caporossi D, Pigozzi F, Sabatini S (eds) Free radicals, health and lifestyle. Medimond Srl, Bologna, pp 37–45Google Scholar
  4. 4.
    Zarkovic N (2003) 4-hydroxynonenal as a bioactive marker of pathopysiological processes. Mol Asp Med 24:281–291CrossRefGoogle Scholar
  5. 5.
    Corvino V, Businaro R, Geloso MC et al (2003) S100B protein and 4-hydroxynonenal in the spinal cord of wobbler mice. Neurochem Res 28:341–345PubMedCrossRefGoogle Scholar
  6. 6.
    Zarkovic K (2003) 4-hydroxynonenal and neurodegenerative diseases. Mol Asp Med 24:293–303CrossRefGoogle Scholar
  7. 7.
    Kalmar B, Greensmith L (2009) Induction of heat shock proteins for protection against oxidative stress. Adv Drug Deliv Rev 28:310–318CrossRefGoogle Scholar
  8. 8.
    Boyer IJ (1989) Toxicity of dibutyltin, tributyltin and other organotin compounds to humans and to experimental animals. Toxicology 55:253–298PubMedCrossRefGoogle Scholar
  9. 9.
    Chang LW (1990) The neurotoxicology and pathology of organomercury, organolead, and organotin. J Toxicol Sci Suppl 4:125–151Google Scholar
  10. 10.
    Fortemps E, Amand G, Bomboir A et al (1978) Trimethyltin poisoning. Report of two cases. Int Arch Occup Environ Health 41:1–6PubMedCrossRefGoogle Scholar
  11. 11.
    Kreyberg S, Torvik A, Bjørneboe A et al (1992) Trimethyltin poisoning: report of a case with postmortem examination. Clin Neuropathol 11:256–259PubMedGoogle Scholar
  12. 12.
    Ross WD, Emmett EA, Steiner J et al (1981) Neurotoxic effects of occupational exposure to organotins. Am J Psychiatry 138:1092–1095PubMedGoogle Scholar
  13. 13.
    Saary MJ, House RA (2002) Preventable exposure to trimethyltin chloride: a case report. Occup Med 52:227–230CrossRefGoogle Scholar
  14. 14.
    Yoo CI, Kim Y, Jeong KS et al (2007) A case of acute organotin poisoning. J Occup Health 49:305–310PubMedCrossRefGoogle Scholar
  15. 15.
    Geloso MC, Corvino V, Michetti F (2011) Trimethyltin-induced hippocampal degeneration as a tool to investigate neurodegenerative processes. Neurochem Int. doi: 10.1016/j.neuint.2011.03.009
  16. 16.
    Balaban CD, O’Callaghan JP, Billingsley ML (1988) Trimethyltin-induced neuronal damage in the rat brain: comparative studies using silver degeneration stains, immunocytochemistry and immunoassay for neurotypic and gliotypic proteins. Neuroscience 26:337–361PubMedCrossRefGoogle Scholar
  17. 17.
    Chang LW, Tiemeyer TM, Wenger GR et al (1982) Neuropathology of mouse hippocampus in acute trimethyltin intoxication. Neurobehav Toxicol Teratol 4:149–156PubMedGoogle Scholar
  18. 18.
    Chang LW, Dyer RS (1983) A time course study of trimethyltin induced neuropathology in rats. Neurobehav Toxicol Teratol 5:443–459PubMedGoogle Scholar
  19. 19.
    Harry GJ, Lefebvre d’Hellencourt C (2003) Dentate gyrus: alterations that occur with hippocampal injury. Neurotoxicology 24:343–356PubMedCrossRefGoogle Scholar
  20. 20.
    O’Callagan JP, Niedwiecke DM, Means JC (1989) Variations in the neurotoxic potency of trimethyltin. Brain Res Bull 2:637–642Google Scholar
  21. 21.
    Chang LW (1986) Neuropathology of trimethyltin: a proposed pathogenetic mechanism. Fundam Appl Toxicol 6:217–232PubMedCrossRefGoogle Scholar
  22. 22.
    Ekuta JE, Hikal AH, Matthews JC (1998) Toxicokinetics of trimethyltin in four inbred strains of mice. Toxicology Lett 95:41–96CrossRefGoogle Scholar
  23. 23.
    Geloso MC, Vinesi P, Michetti F (1996) Parvalbumin-immunoreactive neurons are not affected by trimethyltin-induced neurodegeneration in the rat hippocampus. Exp Neurol 139:269–277PubMedCrossRefGoogle Scholar
  24. 24.
    Geloso MC, Vinesi P, Michetti F (1997) Calretinin-containing neurons in trimethyltin-induced neurodegeneration in the rat hippocampus. An immunocytochemical study. Exp Neurol 146:67–73PubMedCrossRefGoogle Scholar
  25. 25.
    Geloso MC, Vinesi P, Michetti F (1998) Neuronal subpopulations of developing rat hippocampus containing different calcium-binding proteins behave distinctively in trimethyltin-induced neurodegeneration. Exp Neurol 154:645–653PubMedCrossRefGoogle Scholar
  26. 26.
    Brabeck C, Michetti F, Geloso MC et al (2002) Expression of EMAP-II activated monocytes/microglial cells in different regions of the rat hippocampus after trimethyltin-induced brain damage. Exp Neurol 177:341–346PubMedCrossRefGoogle Scholar
  27. 27.
    Geloso MC, Vercelli A, Corvino V et al (2002) Cyclooxygenase-2 and caspase-3 expression in trimethyltin-induced apoptosis in the mouse hippocampus. Exp Neurol 175:152–160PubMedCrossRefGoogle Scholar
  28. 28.
    Geloso MC, Corvino V, Cavallo V et al (2004) Expression of astrocytic nestin in the rat hippocampus during trimethyltin-induced neurodegeneration. Neurosci Lett 357:103–106PubMedCrossRefGoogle Scholar
  29. 29.
    Pompili E, Nori SL, Geloso MC et al (2004) Trimethyltin-induced differential expression of PAR subtypes in reactive astrocytes of the rat hippocampus. Brain Res Mol Brain Res 122:93–98PubMedCrossRefGoogle Scholar
  30. 30.
    Rohl C, Sievers J (2005) Microglia is activated by astrocytes in trimethyltin intoxication. Toxicol Appl Pharm 204:36–45CrossRefGoogle Scholar
  31. 31.
    Harry GJ, Funk JA, Lefebvre d’Hellencourt C et al (2008) The type 1 interleukin 1 receptor is not required for the death of murine hippocampal dentate granule cells and microglia activation. Brain Res 1194:8–20PubMedCrossRefGoogle Scholar
  32. 32.
    Maier EW, Brown HW, Tilson HA et al (1995) Trimethyltin increases interleukin (IL)-1 alpha, IL-6, and Tumor necrosis factor alpha mRNA levels in rat hippocampus. J Neuroimmunol 59:65–75PubMedCrossRefGoogle Scholar
  33. 33.
    Koczyk D (1996) How does trimethyltin affect the brain: facts and hypotheses. Acta Neurobiol Exp 56:587–596Google Scholar
  34. 34.
    Piacentini R, Gangitano C, Ceccariglia S et al (2008) Dysregulation of intracellular calcium homeostasis is responsible for neuronal death in an experimental model of selective hippocampal degeneration induced by trimethyltin. J Neurochem 105:2109–2121PubMedCrossRefGoogle Scholar
  35. 35.
    Jenkins SM, Barone S Jr (2004) The neurotoxicant trimethyltin induces apoptosis via caspase activation, p38 protein kinase, and oxidative stress in PC12 cells. Toxicol Lett 147:63–72PubMedCrossRefGoogle Scholar
  36. 36.
    Yoneyama M, Iwamoto N, Nagashima R et al (2008) Altered expression of heat shock protein 110 family members in mouse hippocampal neurons following trimethyltin treatment in vivo and in vitro. Neuropharmacology 55:693–703PubMedCrossRefGoogle Scholar
  37. 37.
    Yoneyama M, Nishiyama N, Shuto N et al (2008) In vivo depletion of endogenous glutathione facilitates trimethyltin-induced neuronal damage in the dentate gyrus of mice by enhancing oxidative stress. Neurochem Int 52:761–769PubMedCrossRefGoogle Scholar
  38. 38.
    Shuto M, Higuchi K, Sugiyama C et al (2009) Endogenous and esogenous glucocorticoids prevent trimethyltin from causing neuronal degeneration in the mouse brain in vivo: involvement of oxidative stress pathway. J. Pharmacol. Sci. 110:424–436PubMedCrossRefGoogle Scholar
  39. 39.
    Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, San DiegoGoogle Scholar
  40. 40.
    Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247PubMedCrossRefGoogle Scholar
  41. 41.
    Geloso MC, Giannetti S, Cenciarelli C et al (2007) Transplantation of foetal neural stem cells into the rat hippocampus during trimethyltin-induced neurodegeneration. Neurochem Res 32:2054–2061PubMedCrossRefGoogle Scholar
  42. 42.
    Waeg G, Dimsity G, Esterbauer H (1996) Monoclonal antibodies for detection of 4-hydroxynonenal modified proteins. Free Radic Res 25:149–159PubMedCrossRefGoogle Scholar
  43. 43.
    Spickett CM, Wiswedel I, Siems W et al (2010) Advances in methods for the determination of biologically relevant lipid peroxidation products. Free Radic Res 44:1172–1202PubMedCrossRefGoogle Scholar
  44. 44.
    Corvino V, Geloso MC, Cavallo V et al (2005) Enhanced neurogenesis during trimethyltin-induced neurodegeneration in the hippocampus of the adult rat. Brain Res Bull 65:471–477PubMedCrossRefGoogle Scholar
  45. 45.
    Latini L, Geloso MC, Corvino V et al (2010) TMT intoxication induces expression of NOS in neurons and of P2X2R in astrocytes in the hippocampus. J Neurosci Res 88:500–509PubMedGoogle Scholar
  46. 46.
    Negre-Salvayre A, Auge N, Ayala V et al (2010) Pathological aspects of lipid peroxidation. Free Radic Res 44:1125–1171PubMedCrossRefGoogle Scholar
  47. 47.
    Zarkovic N, Ilic Z, Jurin M et al (1993) Stimulation of HeLa cell growth by physiological concentrations of 4-hydroxynonenal. Cell Biochem Funct 11:279–286PubMedCrossRefGoogle Scholar
  48. 48.
    Kruman I, Bruce-Keller AJ, Bredesen D et al (1997) Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J Neuriosci 17:5089–5100Google Scholar
  49. 49.
    Mattson MP, Haddon RC, Rao AM (2000) Molecular functionalization of carbon nanotubes and use as substrates for neuronal growth. J Mol Neurosci 14:175–182PubMedCrossRefGoogle Scholar
  50. 50.
    Yelisyeyeva O, Cherkas A, Zarkovic K et al (2008) The distribution of 4-hydroxynonenal-modified proteins in gastric mucosa of duodenal peptic ulcer patients. Free Radic Res 42:205–211PubMedCrossRefGoogle Scholar
  51. 51.
    Srividhya R, Zarkovic K, Stroser M et al (2009) Mitochondrial alterations in aging rat brain: effective role of (-)- epigallo catechin gallate. Int J Dev Neurosci 27:223–231PubMedCrossRefGoogle Scholar
  52. 52.
    Marquez-Quiñones A, Cipak A, Zarkovic K et al (2010) HNE-protein adducts formation in different pre-carcinogenic stages of hepatitis in LEC rats. Free Radi Res 44:119–127CrossRefGoogle Scholar
  53. 53.
    Hylander BL, Chen X, Graf PC et al (2000) The distribution and localization of hsp110 in brain. Brain Res 869:49–55PubMedCrossRefGoogle Scholar
  54. 54.
    Andersson H, Wetmore C, Lindqvist E et al (1997) Trimethyltin exposure in the rat induces delayed changes in brain-derived neurotrophic factor, c-fos and heat shock protein 70. Neurotoxicol 18:147–159Google Scholar
  55. 55.
    Lively S, Brown IR (2008) Extracellular matrix protein SC1/hevin in the hippocampus following pilocarpine-induced status epilepticus. J Neurochem 107:1335–1346PubMedCrossRefGoogle Scholar
  56. 56.
    Shirakawa T, Nakano K, Hachiya NS et al (2007) Temporospatial patterns of COX-2 expression and pyramidal cell degeneration in the rat hippocampus after trimethyltin administration. Neurosci Res 59:117–123PubMedCrossRefGoogle Scholar
  57. 57.
    Takemiya T, Maehara M, Matsumura K et al (2006) Prostaglandin E2 produced by late induced COX-2 stimulates hippocampal neuron loss after seizure in the CA3 region. Neurosci Res 56:103–110PubMedCrossRefGoogle Scholar
  58. 58.
    Takemiya T, Matsumura K, Yamagata K (2007) Roles of prostaglandin synthesis in excitotoxic brain disease. Neurochem Int 51:112–120PubMedCrossRefGoogle Scholar
  59. 59.
    Kawaguchi K, Hickey RW, Rose ME et al (2005) Cyclooxygenase-2 expression is induced in rat brain after kainite-induced seizures and promotes neuronal death in CA3 hippocampus. Brain Res 1050:130–137PubMedCrossRefGoogle Scholar
  60. 60.
    Viviani B, Corsini E, Pesenti M et al (2001) Trimethyltin-activated cycloxygenase stimulates tumor necrosis factor–a release from glial cell through reactive oxygen species. Toxicol Appl Pharmacol 172:93–97PubMedCrossRefGoogle Scholar
  61. 61.
    Block ML, Hong JS (2005) Microglia and inflammation-mediated neurodegeneration: Multiple triggers with a common mechanism. Prog Neurobiol 76:77–98PubMedCrossRefGoogle Scholar
  62. 62.
    Andreoletti O, Levavasseur E, Uro-Coste E et al (2002) Astrocytes accumulate 4-Hydroxynonenal adducts in murine scrapie and humanB Creutzfeldt–Jakob Disease. Neurobiol Dis 11:386–393PubMedCrossRefGoogle Scholar
  63. 63.
    Minghetti L (2004) Cyclooxygenase-2 (COX-2) in inflammatory and degenerative brain diseases. J Neuropathol Exp Neurol 63:901–910Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • V. Corvino
    • 1
  • E. Marchese
    • 1
  • N. Zarkovic
    • 2
  • K. Zarkovic
    • 3
  • M. Cindric
    • 3
  • G. Waeg
    • 4
  • F. Michetti
    • 1
    Email author
  • M. C. Geloso
    • 1
  1. 1.Institute of Anatomy and Cell BiologyUniversità Cattolica del Sacro CuoreRomeItaly
  2. 2.Division of Molecular MedicineLaboratory for Oxidative Stress, Rudjer Boskovic InstituteZagrebCroatia
  3. 3.Department of Pathology, Neuropathology UnitUniversity of Zagreb School of Medicine, University Hospital CenterZagrebCroatia
  4. 4.Institute of Molecular BiosciencesKarl Franzens University of GrazGrazAustria

Personalised recommendations