Environmental Science and Pollution Research

, Volume 22, Issue 24, pp 20000–20006 | Cite as

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

  • K. Umaa Rani
  • M. Saiyad Musthafa
  • Mehrajuddin War
  • Mohammad K. Al-Sadoon
  • Bilal Ahmad Paray
  • T. H. Mohamed Ahadhu Shareef
  • P. Mohideen Askar Nawas
Research Article
First Online:
Received:
Accepted:

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.

Keywords

TBT Spermatozoa SOD GPx: GR Comet assay 

Notes

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.

References

  1. Agarwal A, Saleh RA, Bedaiwy MA (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79:829–843CrossRefGoogle Scholar
  2. Aitken RJ, Baker MA (2004) Oxygene stress and male reproductive biology. Reprod Fertil Dev 16:581–588CrossRefGoogle Scholar
  3. Alvarez JG, Storey BT (1983) Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility. Biol Reprod 29:548–555CrossRefGoogle Scholar
  4. Alzieu C (2000) Impact of tributyltin on marine invertebrates. Ecotox 9:71–76CrossRefGoogle Scholar
  5. 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. ThesisGoogle Scholar
  6. 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):869–880CrossRefGoogle Scholar
  7. 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 236:231–237Google Scholar
  8. Ballachey BE, Hohenboken WD, Evenson DP (1987) Heterogeneity of sperm nuclear chromatin structure and its relationship to bull fertility. Biol Reprod 36:915–925CrossRefGoogle Scholar
  9. 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 15:1338–1344CrossRefGoogle Scholar
  10. Bentivegna CS, Piatkowski T (1998) Effects of tributyltin on medaka (Oryzias latipes) embryos at different stages of development. Aquat Toxicol 44:117–128CrossRefGoogle Scholar
  11. 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):1027–1032CrossRefGoogle Scholar
  12. Carlberg I, Mannervik B (1975) Purification and characterization of flavoenzyme glutathione reductase from rat liver. Biol Chem 250:5475–5480Google Scholar
  13. 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 86:163–173CrossRefGoogle Scholar
  14. 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 5:158–169Google Scholar
  15. 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 2:152–159CrossRefGoogle Scholar
  16. Collins AR (2004) The COMET assay for DNA damage and repair: principles, applications, and limitations. Mol Biotechnol 26(3):249–261CrossRefGoogle Scholar
  17. de Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C (1997) Reactive oxygen species and sperm physiology. Rev Reprod 2:48–54CrossRefGoogle Scholar
  18. 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 59:221Google Scholar
  19. 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 13:368–378Google Scholar
  20. 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 19:585–594Google Scholar
  21. 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 22:856–870CrossRefGoogle Scholar
  22. Duke RC, Cohen JJ (1986) Endogenous endonuclease-induced DNA fragmentation: an early event in cell-mediated cytolisis. Proc Natl Acad Sci U S A 80:61–63Google Scholar
  23. 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 41:637–651CrossRefGoogle Scholar
  24. Evenson DP, Darzynkiewicz Z, Melamed MR (1980) Relationship of mammalian sperm chromatin heterogenity to fertility. Science 210:1131–1133CrossRefGoogle Scholar
  25. Fent K (1996) Ecotoxicology of organotin compounds. Cri Rev Toxico 26:1–117Google Scholar
  26. Fent K, Meier W (1994) Effects of tributyltin on fish early lifestages. Arch Environ Contam Toxicol 27:224–231CrossRefGoogle Scholar
  27. Gi BK, Richard FL (2004) Effects of genotoxic compounds on DNA and development of early and late grass shrimp embryo stages. Mar Environ Res 57:329–338CrossRefGoogle Scholar
  28. 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 969:244–247CrossRefGoogle Scholar
  29. Gooding MP, Gallardo CS, Leblanc GA (1999) Imposex in three marine gastropod species in Chile and potential impact on muriciculture. Mar Poll Bull 38:1227–1231CrossRefGoogle Scholar
  30. 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 6:141–179Google Scholar
  31. Halliwell B, Gutteridge JMC (1985) Free Radicals in Biology and Medicine. Clarendon, UK, OxfordGoogle Scholar
  32. Harrison PG (1989) Chemistry of Tin. Blackies & Son Ltd., First PublishedGoogle Scholar
  33. 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 169:25–35CrossRefGoogle Scholar
  34. 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 23:1276–1281CrossRefGoogle Scholar
  35. 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 31:531–537Google Scholar
  36. 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 110:13–24CrossRefGoogle Scholar
  37. 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 60:397–404CrossRefGoogle Scholar
  38. Lahnsteiner F, Mansour N, Plaetzer K (2010) Antioxidant systems of brown trout (Salmotrutta fario) semen. AnimalReproduction Science 119:314–321Google Scholar
  39. 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 20:69–79CrossRefGoogle Scholar
  40. Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium deficient rat liver. Biochem Biophys Res Commun 71:952–958CrossRefGoogle Scholar
  41. Li P, Hulak M, Linhart O (2009) Sperm proteins in teleostean and chondrostean (sturgeon) fishes. Fish Physiol Biochem 35:567–581CrossRefGoogle Scholar
  42. Li P, Wei Q, Liu L (2008) DNA integrity of Polyodonspathula cryopreserved sperm. J Appl Ichthyol 24:121–125CrossRefGoogle Scholar
  43. 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 8:416–418Google Scholar
  44. MacLeod J (1943) The role of oxygen in the metabolism and motility of human spermatozoa. Am J Physiol 138:512–518Google Scholar
  45. 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 471:21–27CrossRefGoogle Scholar
  46. Marklund S, Marklund G (1974) Involvement of superoxidation on radical in autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474CrossRefGoogle Scholar
  47. Meador JP (1997) Comparative toxicokinetics of tributyltin in five marine species and its utility in predicting bioaccumulation and acute toxicity. Aqua Toxicol 37(4):307–326CrossRefGoogle Scholar
  48. Merian, E., Anke, M., Ihnat, M., Stoeppler, M., (2004). Elements and their compounds in the environment. 2, WILEY-VCH verlag GmbH & Co. KGaa, Weinheim.Google Scholar
  49. 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 24:591–596CrossRefGoogle Scholar
  50. 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 18:717–721CrossRefGoogle Scholar
  51. Ostling O, Johanson KJ (1984) Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem Biophys Res Commun 123:291–298CrossRefGoogle Scholar
  52. 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 19:235–240CrossRefGoogle Scholar
  53. 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.Google Scholar
  54. 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/s00128-014-1332-4Google Scholar
  55. Rudel H (2003) Case study: bioavailability of tin and tin compounds. Ecotoxicol Environ Saf 56:180–189CrossRefGoogle Scholar
  56. 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):313–320Google Scholar
  57. Shen HM, Chia SE, Ong CN (1999) Evaluation of oxidative DNA damage in human sperm and its association with male infertility. J Androl 20:718–723Google Scholar
  58. 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 1:245–248CrossRefGoogle Scholar
  59. Sikka SC (1996) Oxidative stress and role of antioxidants in normal and abnormal sperm function. Front Biosci 1:78–86Google Scholar
  60. Sikka SC (2001) Relative impact of oxidative stress on male reproductive function. Curr Med Chem 8:851–862CrossRefGoogle Scholar
  61. 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 175:184–191Google Scholar
  62. 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 422:323–330CrossRefGoogle Scholar
  63. Storey KB (1996) Oxidative stress: animal adaptations in nature. Braz J Med Biol Res 29:1715–1733Google Scholar
  64. Sun JG, Juriscova A, Casper RF (1997) Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 56:602–607CrossRefGoogle Scholar
  65. 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 38:1–27CrossRefGoogle Scholar
  66. 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.Google Scholar
  67. Tremellen K (2008) Oxidative stress and male infertility—a clinical perspective. Hum Reprod Update 14:243–258CrossRefGoogle Scholar
  68. 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 254:758–767CrossRefGoogle Scholar
  69. 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 193:303–309CrossRefGoogle Scholar
  70. Waldock MJ, Thain J (1983) Shell thickening in Crassostrea gigas: organotin antifouling or sediment-induced. Mar Poll Bull 14:411–415CrossRefGoogle Scholar
  71. Wishart GJ (1984) Effects of lipid peroxide formation in fowl semen on sperm motility, ATP content and fertilizing ability. J Reprod Fert 71:113–118CrossRefGoogle Scholar
  72. 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 17:281–284Google Scholar
  73. Xu XC, Ding FH, Li J (2005) Cryopreservation caused sperm DNA damage in red sea bream Pagrosomus major and its detection. Oceanol Limnol Sin 36:221–225Google Scholar
  74. 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 77:136–142CrossRefGoogle Scholar
  75. Zilli L, Schiavone R, Zonno V, Storelli C, Vilella S (2003) Evaluation of DNA damage in Dicentrarchus labrax sperm following cryopreservation. Cryobiol 47:227–235CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • K. Umaa Rani
    • 1
  • M. Saiyad Musthafa
    • 2
  • Mehrajuddin War
    • 2
  • Mohammad K. Al-Sadoon
    • 3
  • Bilal Ahmad Paray
    • 3
  • T. H. Mohamed Ahadhu Shareef
    • 4
  • P. Mohideen Askar Nawas
    • 5
  1. 1.Department of BiotechnologySri Sankara Arts and Science CollegeKancheepuramIndia
  2. 2.P.G. & Research Department of ZoologyThe New CollegeChennaiIndia
  3. 3.Department of ZoologyCollege of Science, King Saud UniversityRiyadhSaudi Arabia
  4. 4.Department of ChemistryThe New CollegeChennaiIndia
  5. 5.P.G. & Research Department of ZoologyPeriyar E.V.R College of Arts and ScienceTrichirappalliIndia

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