Skip to main content
SpringerLink
Log in

Impact of tributyltin on antioxidant and DNA damage response in spermatozoa of freshwater prawn Macrobrachium rosenbergii

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Effects of tributyltin (TBT) on antioxidant [total superoxide dismutase (SOD), glutathione peroxidase (GPx), and glutathione reductase (GR)] and DNA damage levels in the spermatozoa were studied and reported here for the first time in the freshwater prawn Macrobrachium rosenbergii. Three groups of (n = 10 in each group) fishes were exposed to three different nominal concentrations of TBT viz., 1, 2, and 4 mg L−1 along with control group for 90 days. Significant decrease of antioxidant and increased DNA damage levels were seen at higher doses of 2 and 4 mg L−1. In prawn, the antioxidant level plays a vital role in sperm protection, activation, differential functions related to the physiology, and reproductive behavior. This study serves as a biomonitoring tool to assess the TBT effects on reproductive behavior of aquatic biota.

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

Similar content being viewed by others

References

  • Agarwal A, Saleh RA, Bedaiwy MA (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79:829–843

    Article  Google Scholar 

  • Aitken RJ, Baker MA (2004) Oxygene stress and male reproductive biology. Reprod Fertil Dev 16:581–588

    Article  CAS  Google Scholar 

  • Alvarez JG, Storey BT (1983) Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility. Biol Reprod 29:548–555

    Article  CAS  Google Scholar 

  • Alzieu C (2000) Impact of tributyltin on marine invertebrates. Ecotox 9:71–76

    Article  CAS  Google Scholar 

  • Amr FA (2004) Biological studies on the use of some invertebrates as bioindicator of pollution by one of oil derivatives. Faculty of Science, Al-Azhar University, Egypt, M.Sc. Thesis

    Google Scholar 

  • Armstrong JS, Rajasekaran M, Chamulitrat W, Gatti P, Hellstrom WJ, Sikka SC (1999) Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism. Free Rad Biol Med 26(7–8):869–880

    Article  CAS  Google Scholar 

  • Aravindan GR, Bjordahl J, Jost LK, Evenson DP (1997) Susceptibility of human sperm to in situ denaturation is strongly correlated with DNA strand breaks identified by single-cell electrophoresis. Exp Cell Res 236:231–237

  • Ballachey BE, Hohenboken WD, Evenson DP (1987) Heterogeneity of sperm nuclear chromatin structure and its relationship to bull fertility. Biol Reprod 36:915–925

    Article  CAS  Google Scholar 

  • Barroso G, Morshedi M, Oehninger S (2000) Analysis of DNA fragmentation plasma membrane translocation of phosphatidyl serine and oxidative stress in human spermatozoa. Hum Reprod 15:1338–1344

    Article  CAS  Google Scholar 

  • Bentivegna CS, Piatkowski T (1998) Effects of tributyltin on medaka (Oryzias latipes) embryos at different stages of development. Aquat Toxicol 44:117–128

    Article  CAS  Google Scholar 

  • Bushong SJ, Hall LW Jr, Hall WS, Johnson WE, Herman RL (1988) Acute toxicity of tributyltin to selected Chesapeake Bay fish and invertebrates. Water Res 22(8):1027–1032

    Article  CAS  Google Scholar 

  • Carlberg I, Mannervik B (1975) Purification and characterization of flavoenzyme glutathione reductase from rat liver. Biol Chem 250:5475–5480

    CAS  Google Scholar 

  • Cassani P, Beconi MT, O’Flaherty C (2005) Relationship between total superoxide dismutase activity with lipid peroxidation, dynamics and morphological parameters in canine semen. Anim Reprod Sci 86:163–173

    Article  CAS  Google Scholar 

  • Catharios JC, Alambritis G, Miliou H, Cotou E, Zouganelis GD (2014) Comparative toxicity of “tin free” self-polishing copolymer antofouling paints and their inhibitory effects on larval development of a non-target organism. Mate Sci & Appli 5:158–169

    Google Scholar 

  • Cheema RS, Bansal AK, Bilaspuri GS (2009) Manganeseprovides antioxidant protection for sperm cryopreservation that may offer new consideration for clinical fertility. Oxid Med Cell Longev 2:152–159

    Article  Google Scholar 

  • Collins AR (2004) The COMET assay for DNA damage and repair: principles, applications, and limitations. Mol Biotechnol 26(3):249–261

    Article  CAS  Google Scholar 

  • de Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C (1997) Reactive oxygen species and sperm physiology. Rev Reprod 2:48–54

    Article  Google Scholar 

  • deLamirande E, Gagnon C (1993) Human sperm hyper activation in whole semen and its association with low superoxide scavenging capacity in seminal plasma and spermatozoa. Fertil Steril 59:221

    Google Scholar 

  • deLamirande E, Gagnon C (1992) Reactive oxygen species and human spermatozoa. I. Effect on the motility of intact spermatoz oa and on sperm axonemes. J Androl 13:368–378

    CAS  Google Scholar 

  • deLamirande E, Tsai C, Harakat A, Gagnon C (1998) Involvement of reactive oxygen species in human sperm arcosome reaction induced by A23187, lysophosphatidylcholine, and biological fluid ultra filtrates. J Androl 19:585–594

    CAS  Google Scholar 

  • Domínguez-Rebolledo ÁE, Fernández-Santos MR, Bisbal A, Ros-Santaella JL, Ramón M, Carmona M (2010) Improving the effect of incubation and oxidative stress on thawed spermatozoa from red deer by using different antioxidant treatments. Reprod Fertil Dev 22:856–870

    Article  Google Scholar 

  • Duke RC, Cohen JJ (1986) Endogenous endonuclease-induced DNA fragmentation: an early event in cell-mediated cytolisis. Proc Natl Acad Sci U S A 80:61–63

    Google Scholar 

  • Evenson DP, Thompson L, Jost. L (1994) Flow cytometric evaluation of boar semen by the sperm chromatin structure assay as related to cryopreservation and fertility. Theriogenology 41:637–651

    Article  CAS  Google Scholar 

  • Evenson DP, Darzynkiewicz Z, Melamed MR (1980) Relationship of mammalian sperm chromatin heterogenity to fertility. Science 210:1131–1133

    Article  CAS  Google Scholar 

  • Fent K (1996) Ecotoxicology of organotin compounds. Cri Rev Toxico 26:1–117

    CAS  Google Scholar 

  • Fent K, Meier W (1994) Effects of tributyltin on fish early lifestages. Arch Environ Contam Toxicol 27:224–231

    Article  CAS  Google Scholar 

  • Gi BK, Richard FL (2004) Effects of genotoxic compounds on DNA and development of early and late grass shrimp embryo stages. Mar Environ Res 57:329–338

    Article  Google Scholar 

  • Giovannelli L, Decorosi F, Dolara P, Pulvirenti L (2003) Vulnerability to DNA damage in the aging rat substantia nigra: a study with the comet assay. Brain Res 969:244–247

    Article  CAS  Google Scholar 

  • Gooding MP, Gallardo CS, Leblanc GA (1999) Imposex in three marine gastropod species in Chile and potential impact on muriciculture. Mar Poll Bull 38:1227–1231

    Article  CAS  Google Scholar 

  • Hall W Jr, Scott MC, Killen WD, Unger MA (2000) A probabilistic ecological risk assessment of tributyltin in surface waters of the Chesapeake Bay watershed. Human Ecol 6:141–179

    CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1985) Free Radicals in Biology and Medicine. Clarendon, UK, Oxford

    Google Scholar 

  • Harrison PG (1989) Chemistry of Tin. Blackies & Son Ltd., First Published

    Google Scholar 

  • Homma-Takeda S, Kugenuma Y, Iwamuro T, Kumagai Y, Shimojo N (2001) Impairment of spermatogenesis in rats by methylmercury: involvement of stage- and cell-specific germ cell apoptosis. Toxicology 169:25–35

    Article  CAS  Google Scholar 

  • Inoue S, Oshima Y, Nagai K, Yammoto T, Go J, Kai N, Honja T (2004) Effect of maternal exposure to tributyltin on reproduction of the pearl oyster (Pinctada fucata martensii). Environ Toxicol Chem 23:1276–1281

    Article  CAS  Google Scholar 

  • Jones R, Mann T, Sherins R (1979) Peroxidative breakdown of phospholipids inhuman spermatozoa, spemicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fert Steril 31:531–537

    CAS  Google Scholar 

  • Koppen G, Toncelli TM, Triest L, Verschaeve L (1999) The comet assay: a tool to study alterations of DNA integrity in developing plant leaves. Mech Age Develop 110:13–24

    Article  CAS  Google Scholar 

  • Labbe C, Martoriati A, Devaux A, Maisse G (2001) Effect of sperm cryopreservation on sperm DNA stability and progeny development in rainbow trout. Mol Reprod Develop 60:397–404

    Article  CAS  Google Scholar 

  • Lahnsteiner F, Mansour N, Plaetzer K (2010) Antioxidant systems of brown trout (Salmotrutta fario) semen. AnimalReproduction Science 119:314–321

    CAS  Google Scholar 

  • Laughlin RB, Franch WJ, Guard HF (1983) Acute and sub lethal toxicity of tributyltin oxide (TBTO) and its putative environmental product, tributyltin sulfide (TBTS) to zoeal mud crabs. Water Air Soil Pollu 20:69–79

    Article  CAS  Google Scholar 

  • Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium deficient rat liver. Biochem Biophys Res Commun 71:952–958

    Article  CAS  Google Scholar 

  • Li P, Hulak M, Linhart O (2009) Sperm proteins in teleostean and chondrostean (sturgeon) fishes. Fish Physiol Biochem 35:567–581

    Article  CAS  Google Scholar 

  • Li P, Wei Q, Liu L (2008) DNA integrity of Polyodonspathula cryopreserved sperm. J Appl Ichthyol 24:121–125

    Article  Google Scholar 

  • Lu H, Zhang L, Zhang N, Tang J, Ding XP, Tang Y (2002) Detection of DNA damage of human sperm using single cell electrophoresis. Zhonghua Nan Ke Xue 8:416–418

    CAS  Google Scholar 

  • MacLeod J (1943) The role of oxygen in the metabolism and motility of human spermatozoa. Am J Physiol 138:512–518

  • Maluf SW, Erdtmann B (2000) Follow-up study of the genetic damage in lymphocytes of pharmacists and nurses handling antineoplastic drugs evaluated by cytokinesis-block micronuclei analysis and single cell gel electrophoresis assay. Mut Res 471:21–27

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Meador JP (1997) Comparative toxicokinetics of tributyltin in five marine species and its utility in predicting bioaccumulation and acute toxicity. Aqua Toxicol 37(4):307–326

    Article  CAS  Google Scholar 

  • Merian, E., Anke, M., Ihnat, M., Stoeppler, M., (2004). Elements and their compounds in the environment. 2, WILEY-VCH verlag GmbH & Co. KGaa, Weinheim.

  • Nakayama K, Oshima Y, Nagafuchi K, Hano T, Shimasaki Y, Honjo T (2005) Early-life-stage toxicity in offspring from exposed parent medaka, Oryzias latipes, to mixtures of tributyltin and polychlorinated biphenyls. Environ Toxicol Chem 24:591–596

    Article  CAS  Google Scholar 

  • Nirmala K, Oshima Y, Lee R, Imada N, Honja T, Kobayashi K (1999) Transgenerational toxicity of tributyltin and its combined effects with polychlorinated biphenyls on reproductive process in Japanese medaka (Oryzia slatipes). Environ Toxicol Chem 18:717–721

    Article  CAS  Google Scholar 

  • Ostling O, Johanson KJ (1984) Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem Biophys Res Commun 123:291–298

    Article  CAS  Google Scholar 

  • Pinkney AE, Matteson LL, Wright DA (1990) Effects of tributyltin on survival, growth, morphometry, and RNA-DNA ratio of larval striped bass, Morones axatilis. Arch Environ Contam Toxicol 19:235–240

    Article  CAS  Google Scholar 

  • Revathi, P., Palanisamy Iyapparaj, Lourduraj Arockia Vasanthi, Natesan Munuswamy, Muthukalingan Krishnan., (2012). Ultrastructural changes during spermatogenesis, biochemical and hormonal evidences of testicular toxicity caused by TBT in freshwater prawn Macrobrachium rosenbergii (De Man, 1879). Environmental Toxicology. 1–11.

  • Revathi, P., Palanisamy Iyapparaj, Lourduraj Arockia Vasanthi, Natesan Munuswamy, Vimalanathan Arun Prasanna, Jayaraj Pandiyarajan, Muthukalingan Krishnan., (2014). Influence of short term exposure of tbt on the male reproductive activity in freshwater prawn Macrobrachium rosenbergii (De Man). Bull Environ Contam Toxicol. DOI 10.1007/s00128-014-1332-4

  • Rudel H (2003) Case study: bioavailability of tin and tin compounds. Ecotoxicol Environ Saf 56:180–189

    Article  CAS  Google Scholar 

  • Shaliutina AK, Gazo I, Cosson J, Linhart O (2013) Comparison of oxidant and antioxidant status of seminal plasma and spermatozoa of several fish species. Czeh J Anim Sci 58(7):313–320

    Google Scholar 

  • Shen HM, Chia SE, Ong CN (1999) Evaluation of oxidative DNA damage in human sperm and its association with male infertility. J Androl 20:718–723

    CAS  Google Scholar 

  • Shimasaki Y, Kitano T, Osihma Y, Inoue S, Inoue Y, Kang IJ, Nakayama KM, Honjo T (2006) Effect of trubutyltin on reproduction in Japanese whiting, Sillago japonica. Mar Environ Res 1:245–248

    Article  Google Scholar 

  • Sikka SC (1996) Oxidative stress and role of antioxidants in normal and abnormal sperm function. Front Biosci 1:78–86

    Google Scholar 

  • Sikka SC (2001) Relative impact of oxidative stress on male reproductive function. Curr Med Chem 8:851–862

    Article  CAS  Google Scholar 

  • Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191

  • Stavreva DA, Ptacek O, Plewa MJ, Gichner T (1998) Single cell gel electrophoresis analysis of genomic damage induced by ethyl methane sulfonate in cultured tobacco cells. Mut Res 422:323–330

    Article  CAS  Google Scholar 

  • Storey KB (1996) Oxidative stress: animal adaptations in nature. Braz J Med Biol Res 29:1715–1733

    CAS  Google Scholar 

  • Sun JG, Juriscova A, Casper RF (1997) Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 56:602–607

    Article  CAS  Google Scholar 

  • Surai PF, Speake BK, Sparks NH (2001) Carotenoids in avian nutrition and embryonic in plasma development. 1. Absorption, availability and levels in plasma and egg yolk. J Poult Sci 38:1–27

    Article  CAS  Google Scholar 

  • Surai, P., Cerolini, S., Maldjian, A., Noble, R., Speake, B., (1998). Effect of lipid peroxidation on the phospholipid and fatty acid composition of turkey spermatozoa: a protective effect of vitamin E. In: Lauria, A., Gandolfi, F., Enne, G., Gianaroli, L. (Eds.), I. Gametes: Development and Function, 50th International Congress on Animal Reproduction. Milano. 603.

  • Tremellen K (2008) Oxidative stress and male infertility—a clinical perspective. Hum Reprod Update 14:243–258

    Article  CAS  Google Scholar 

  • Trenzado C, Hidalgo MC, García-Gallego M, Morales AE, Furné M, Domezain A, Domezain J, Sanz A (2006) Antioxidantenzymes and lipid peroxidation in sturgeon Acipenser naccarii and trout Oncorhynchus mykiss. A comparative study. Aquaculture 254:758–767

    Article  CAS  Google Scholar 

  • Van Loon AAWM, Den Boer PJ, van der Schans GP (1991) Immunochemical detection of DNA damage induction and repair at different cellular stages of spermatogenesis of the hamster after in vitro or in-vivo exposure to ionizing radiation. Exp Cell Res 193:303–309

    Article  Google Scholar 

  • Waldock MJ, Thain J (1983) Shell thickening in Crassostrea gigas: organotin antifouling or sediment-induced. Mar Poll Bull 14:411–415

    Article  CAS  Google Scholar 

  • Wishart GJ (1984) Effects of lipid peroxide formation in fowl semen on sperm motility, ATP content and fertilizing ability. J Reprod Fert 71:113–118

    Article  CAS  Google Scholar 

  • Xu DX, Shen HM, Wang JN (2000) Detection of DNA strands breakage in human spermatozoa by use of single-cell gel electrophoresis. China Med Bd NY 17:281–284

    CAS  Google Scholar 

  • Xu XC, Ding FH, Li J (2005) Cryopreservation caused sperm DNA damage in red sea bream Pagrosomus major and its detection. Oceanol Limnol Sin 36:221–225

    CAS  Google Scholar 

  • Zhou B, Liu W, Siu WHL, O’ Toole D, Lam PKS, Wu RSS (2006) Exposure of spermatozoa to duroquinone may impair reproduction of the common carp (Cyprinus carpio) through oxidative stress. Aquat Toxicol 77:136–142

    Article  CAS  Google Scholar 

  • Zilli L, Schiavone R, Zonno V, Storelli C, Vilella S (2003) Evaluation of DNA damage in Dicentrarchus labrax sperm following cryopreservation. Cryobiol 47:227–235

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to express their sincere appreciation to the Deanship of Scientific Research at the King Saud University, Riyadh, Saudi Arabia for funding this Research Group project no RGP-289. The authors are also thankul to Dr. M. Jamal Mohamed, Assistant Professor, P.G & Research Department of Zoology, The New College, Chennai and anonymous reviewers for critical review of this article.

Author information

Authors and Affiliations

  1. Department of Biotechnology, Sri Sankara Arts and Science College, Kancheepuram, Tamil Nadu, India

    K. Umaa Rani

  2. P.G. & Research Department of Zoology, The New College, Chennai, 600014, Tamil Nadu, India

    M. Saiyad Musthafa & Mehrajuddin War

  3. Department of Zoology, College of Science, King Saud University, PO Box 2455, Riyadh, 11451, Saudi Arabia

    Mohammad K. Al-Sadoon & Bilal Ahmad Paray

  4. Department of Chemistry, The New College, Chennai, 600014, Tamilnadu, India

    T. H. Mohamed Ahadhu Shareef

  5. P.G. & Research Department of Zoology, Periyar E.V.R College of Arts and Science, Trichirappalli, Tamil Nadu, India

    P. Mohideen Askar Nawas

Authors
  1. K. Umaa Rani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Saiyad Musthafa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mehrajuddin War
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohammad K. Al-Sadoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bilal Ahmad Paray
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. H. Mohamed Ahadhu Shareef
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. P. Mohideen Askar Nawas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Saiyad Musthafa.

Additional information

Responsible editor: Thomas Hutchinson

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rani, K.U., Musthafa, M.S., War, M. et al. Impact of tributyltin on antioxidant and DNA damage response in spermatozoa of freshwater prawn Macrobrachium rosenbergii . Environ Sci Pollut Res 22, 20000–20006 (2015). https://doi.org/10.1007/s11356-015-5202-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5202-3

Keywords

Search

Navigation