Skip to main content

Advertisement

SpringerLink
Log in

2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces oxidative stress in the epididymis and epididymal sperm of adult rats

  • Molecular Toxicology
  • Published:
Archives of Toxicology Aims and scope Submit manuscript

Abstract

2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) is one of the most potent environmental contaminants, which has been shown to induce oxidative stress in testis and epididymal sperm of rats. However, the nature and mechanism of action of TCDD on the epididymis is not clear. The aim of the present study was to investigate whether induction of oxidative stress in epididymal sperm was direct effect of TCDD on epididymis. In the present studies, TCDD (0.1, 1.0 and 10 µg/kg body weight per day) was administered orally to rats for 4 days. Twenty-four hours after the last treatment the animals were killed using anesthetic ether. Both epididymides were dissected out and epididymal sperm were collected by cutting the epididymides into small pieces in Ham's F-12 medium at 35°C. The epididymal sperm and caput, corpus and cauda epididymides were homogenized and used for biochemical studies. Epididymal sperm counts did not decrease in the rats treated with TCDD. Administration of TCDD increased the production of reactive oxygen species such as hydrogen peroxide while the activities of antioxidant enzymes superoxide dismutase, catalase, glutathione reductase and glutathione peroxidase were found to be decreased in the epididymal sperm as well as in cauda epididymides. Lipid peroxidation also increased in the epididymal sperm and in the various regions of the epididymides after exposure to TCDD. The results indicated that TCDD induces oxidative stress in the epididymis and epididymal sperm by decreasing the antioxidant enzymes through induction of reactive oxygen species. Thus, the adverse effects of TCDD on the epididymal sperm were due to direct effect of TCDD on epididymis.

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

Similar content being viewed by others

References

  • Aitken RJ, Clarkson JS, Hargreave TB (1989) Analysis of the relationship between defective sperm function and the generation of reactive oxygen species in cases of oligozoospermia. J Androl 10:214–220

    CAS  PubMed  Google Scholar 

  • Buege JA, Aust SD (1976) Lactoperoxidase catalyzed lipid peroxidation of microsomal and artificial membranes. Biochim Biophys Acta 444:192–201

    CAS  PubMed  Google Scholar 

  • Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5474–5480

    Google Scholar 

  • Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–534

    CAS  PubMed  Google Scholar 

  • Chitra KC, Sujatha R, Latchoumycandane C, Mathur PP (2001) Effect of lindane on antioxidant enzymes in epididymis and epididymal sperm of adult rats. Asian J Androl 3:205–208

    CAS  PubMed  Google Scholar 

  • Chitra KC, Latchoumycandane C, Mathur PP (2002) Induction of oxidative stress in the epididymal sperm of rat after exposure to nonylphenol. Arch Toxicol 76:545–551

    Article  CAS  PubMed  Google Scholar 

  • Cooper TG (1999) Epididymis. In: Knobil E, Neil JD (eds) Encyclopedia of reproduction, vol 2. Academic Press, San Diego, pp 1–17

  • El-Sabeawy F, Wang S, Overstreet J, Miller M, Lasley B, Enan E (1998) Treatment of rats during pubertal development with 2,3,7,8-tetrachlorodibenzo-p-dioxin alters both signaling kinase activities and epidermal growth factor receptor binding in the testis and the motility and acrosomal reaction of sperm. Toxicol Appl Pharmacol 150:427–442

    Article  CAS  PubMed  Google Scholar 

  • Enan E, El-Sabeawy F, Overstreet J, Matsumura F, Lasley B (1998) Mechanisms of gender-specific TCDD-induced toxicity in guinea pig adipose tissue. Reprod Toxicol 12:357–369

    CAS  PubMed  Google Scholar 

  • Faqi AS, Dalsenter PR, Ligensa A, Merker HJ, Chahoud I (1997) Effect on male fertility and testis concentrations of low dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in offspring of rats exposed during pregnancy and lactation. Teratology 56:403

    Google Scholar 

  • Gray LE Jr, Kelce WR, Monosson E, Ostby JS, Birnbaum LS (1995) Exposure to TCDD during development permanently alters reproductive function in male Long Evans rats and hamsters: reduced ejaculated and epididymal sperm numbers and sex accessory gland weights in offspring with normal androgenic status. Toxicol Appl Pharmacol 131:108–118

    Article  CAS  PubMed  Google Scholar 

  • Gray LE, Ostby JS, Kelce WR (1997) A dose-response analysis of the reproductive effects of a single gestational dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin in male Long Evans Hooded rat offspring. Toxicol Appl Pharmacol 146:11–20

    CAS  PubMed  Google Scholar 

  • Griveau JF, Lannou DL (1997) Reactive oxygen species and human spermatozoa: physiology and pathophysiology. Int J Androl 20:61–69

    PubMed  Google Scholar 

  • Hassoun EA, Li F, Abushaban A, Stohs SJ (2001) Production of superoxide anion, lipid peroxidation and DNA damage in the hepatic and brain tissues of rats after subchronic exposure to mixtures of TCDD and its congeners. J Appl Toxicol 21:211–219

    Article  CAS  PubMed  Google Scholar 

  • Hess RA (1998) Effects of environmental toxicants on the efferent ducts, epididymis and fertility. J Reprod Fertil 53:247–59

    CAS  Google Scholar 

  • Ichikawa T, Oeda T, Ohmori H, Schill WB (1999) Reactive oxygen species influence the acrosome reaction but not acrosin activity in human spermatozoa. Int J Androl 22:37–42

    Article  CAS  PubMed  Google Scholar 

  • Klinefelter GR, Hess RA (1998) Toxicology of the male excurrent ducts and accessory sex glands. In: Korach KS (ed) Reproductive and developmental toxicology. Marcel Decker, New York, pp 553–591

  • Kobayashi T, Miyazaki T, Natori M, Nozawa S (1991) Protective role of superoxide dismutase in human sperm motility: superoxide dismutase activity and lipid peroxide in human seminal plasma and spermatozoa. Hum Reprod 6:987–991

    CAS  PubMed  Google Scholar 

  • Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751–5754

    CAS  PubMed  Google Scholar 

  • Latchoumycandane C, Mathur PP (2002a) Effect of vitamin E on reactive oxygen species mediated 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity in rat testis. J Appl Toxicol 22:345–351

    Article  CAS  PubMed  Google Scholar 

  • Latchoumycandane C, Mathur PP (2002b) Effect of methoxychlor on the antioxidant system of mitochondrial and microsome-rich fractions of rat testis. Toxicology 176:67–75

    CAS  PubMed  Google Scholar 

  • Latchoumycandane C, Mathur PP (2002c) Induction of oxidative stress in the rat testis after short-term exposure to the organochlorine pesticide methoxychlor. Arch Toxicol 76:692–698

    Article  CAS  PubMed  Google Scholar 

  • Latchoumycandane C, Chitra KC, Mathur PP (2002a) The effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the antioxidant system in mitochondrial and microsomal fractions of rat testis. Toxicology 171:127–135

    CAS  PubMed  Google Scholar 

  • Latchoumycandane C, Chitra KC, Mathur PP (2002b) Induction of oxidative stress in the rat epididymal sperm after exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Arch Toxicol 76:113–118

    CAS  PubMed  Google Scholar 

  • Latchoumycandane C, Chitra KC, Mathur PP (2002c) The effect of methoxychlor on the epididymal antioxidant system of adult rats. Reprod Toxicol 16:161–172

    CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Mably TA, Moore RW, Peterson RE (1992) In utero and lactational exposure of male rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 114:97–107

    CAS  PubMed  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of superoxide anion radical in autooxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474

    CAS  PubMed  Google Scholar 

  • Mohammadpour H, Murray WJ, Stohs, JJ (1988) 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD)-induced lipid peroxidation in genetically responsive and non-responsive mice. Arch Environ Contam Toxicol 17:645–650

    CAS  PubMed  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    CAS  PubMed  Google Scholar 

  • Pick E, Keisari Y (1981) Superoxide anion and H2O2 production by chemically elicited peritoneal macrophages-induction by multiple nonphagocytic stimuli. Cell Immunol 59:301–318

    CAS  PubMed  Google Scholar 

  • Safe S (1995) Modulation of gene expression and endocrine response pathways by 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds. Pharmacol Ther 67:247–281

    CAS  PubMed  Google Scholar 

  • Safe S (2001) Molecular biology of the Ah receptor and its role in carcinogenesis. Toxicol Lett 120:1–7

    CAS  PubMed  Google Scholar 

  • Senft AP, Dalton TP, Bebert DW, Genter MB, Hutchinson RJ, Shertzer HG (2002) Dioxin increases reactive oxygen production in mouse liver mitochondria. Toxicol Appl Pharmacol 178:15–21

    Article  CAS  PubMed  Google Scholar 

  • Sharpe RM (1993) Declining sperm counts in men — is there an endocrine cause? J Endocrinol 136:357–360.

    CAS  PubMed  Google Scholar 

  • Sinet PM, Garber P (1981) Inactivation of human Cu–Zn superoxide dismutase during exposure to O2 − and H2O2. Arch Biochem Biophys 212:411–416

    CAS  PubMed  Google Scholar 

  • Skene SA, Dewhurst IC, Greenberg M (1989) Polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans: the risk to human health. A review. Hum Toxicol 8:177–203

    Google Scholar 

  • Stohs SJ (1990) Oxidative stress induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Free Radic Biol Med 9:79–90

    CAS  PubMed  Google Scholar 

  • Sujatha R, Chitra KC, Latchoumycandane C, Mathur PP (2001) Effect of lindane on testicular antioxidant system and steroidogenic enzymes in adult rats. Asian J Androl 3:135–138

    CAS  PubMed  Google Scholar 

  • Williams GM, Iatropoulos (2001) Principles of testing for carcinogenic activity. In: Hayes AW (ed) Principles and methods of toxicology. Raven Press, New York, pp 959–1000

Download references

Acknowledgements

The authors acknowledge Dr. Stephen Safe, Texas, USA, for the generous gift of TCDD, and the staff of the Bioinformatics Center, Pondicherry University for various facilities. C.L. acknowledges the Indian Council of Medical Research, New Delhi, for a Senior Research Fellowship; K.C.C acknowledges Lady Tata Memorial Trust, Mumbai, India, for a Junior Scholarship, and P.P.M. acknowledges the Population Council, New York for financial assistance (Grant Nos. B99.047P-9/ICMC and B99.048R/ICMC).

Author information

Authors and Affiliations

  1. School of Life Sciences, Pondicherry University, Pondicherry, 605 014, India

    C. Latchoumycandane, K. C. Chitra & P. P. Mathur

Authors
  1. C. Latchoumycandane
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. C. Chitra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. P. Mathur
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. P. Mathur.

Additional information

This paper was presented at the 35th Annual Meeting of the Society for the Study of Reproduction, Baltimore, USA, 28–31 July, 2002.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Latchoumycandane, C., Chitra, K.C. & Mathur, P.P. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces oxidative stress in the epididymis and epididymal sperm of adult rats. Arch Toxicol 77, 280–284 (2003). https://doi.org/10.1007/s00204-003-0439-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00204-003-0439-x

Keywords

Search

Navigation