Skip to main content
SpringerLink
Log in

Toxic dinoflagellate Alexandrium tamarense induces oxidative stress and apoptosis in hepatopancreas of shrimp (Fenneropenaeus chinensis)

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

This study investigated the inductive effect of Alexandrium tamarense, a toxic dinoflagellate producing paralytic shellfish poison, on oxidative stress and apoptosis in hepatopancreas of Chinese shrimp, Fenneropenaeus chinensis. The individuals of F. chinensis were exposed to 200 and 1000 cells mL−1 of A. tamarense with their superoxide dismutase (SOD), glutathione S-transferase (GST) activities, malonyldialdehyde (MDA) concentration, and caspase gene (FcCasp) expression in hepatopancreas determined at 12, 24, 48, 72 and 96 h. In addition, apoptosis in hepatopancreas of F. chinensis at 96 h after exposure was determined through terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling (TUNEL) assay. The hepatopancreatic SOD and GST activities of F. chinensis exposed to 1000 cells mL−1 of A. tamarense showed a bell-shaped response to exposure time. The hepatopancreatic MDA concentration of F. chinensis exposed to 1000 cells mL−1 of A. tamarense increased gradually from 48 to 96 h, and such a trend corresponded to the decrease of GST activity. The hepatopancreatic FcCasp transcript abundance of F. chinensis exposed to 1000 cells mL−1 of A. tamarense was positively and linearly correlated to MDA concentration. Results of TUNEL assay showed that exposure to 1000 cells mL−1 of A. tamarense induced apoptosis in the hepatopancreas of F. chinensis. Our study revealed that A. tamarense exposure influenced the antioxidative status of F. chinensis and caused lipid peroxidation and apoptosis in the hepatopancreas of shrimp.

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

  • Alonso-Rodríguez, R., and Páez-Osuna, F., 2003. Nutrients, phytoplankton and harmful algal blooms in shrimp ponds: A review with special reference to the situation in the Gulf of California. Aquaculture, 219: 317–336.

    Article  Google Scholar 

  • Armstrong, J. S., 2006. Mitochondrial membrane permeabilization: The sine qua non for cell death. Bioessays, 28: 253–260.

    Article  Google Scholar 

  • Buikema, A. L., Niederlehner, B. R., and Cairns, J. J., 1982. Biological monitoring, part IV-toxicity testing. Water Research, 16: 239–262.

    Article  Google Scholar 

  • Buttke, T. M. and Sandstrom, P. A., 1994. Oxidative stress as a mediator of apoptosis. Immunology Today, 15: 7–10.

    Article  Google Scholar 

  • Chen, Y., 2008. Toxic effects and mechanisms of Diarrhetic Shellfish Poisoning (DSP) and other HAB toxins on mammalian cells. Ph.D thesis. Chinese Academy of Sciences, 60–69.

    Google Scholar 

  • Costa, P. R., Botelho, M. J., and Lefebvre, K. A., 2010. Characterization of paralytic shellfish toxins in seawater and sardines (Sardina pilchardus) during blooms of Gymnodinium catenatum. Hydrobiologia, 655: 89–97.

    Article  Google Scholar 

  • Costa, P. R., Pereira, P., Guilherme, S., Barata, M., Nicolau, L., Santos, M. A., Pacheco, M., and Pousão-Ferreira, P., 2012. Biotransformation modulation and genotoxicity in white seabream upon exposure to paralytic shellfish toxins produced by Gymnodinium catenatum. Aquatic Toxicology, 106-107, 42–47.

    Article  Google Scholar 

  • Estrada, N., Romero, M. J., Campa-Córdova, A., Luna, A., and Ascencio, F., 2007. Effects of the toxic dinoflagellate, Gymnodinium catenatum on hydrolytic and antioxidant enzymes, in tissues of the giant lions-paw scallop Nodipecten subnodosus. Comparative Biochemistry and Physiology, 146: 502–510.

    Google Scholar 

  • Fleury, C., Mignotte, B., and Vayssiere, J. L., 2002. Mitochondrial reactive oxygen species in cell death signaling. Biochimie, 84: 131–141.

    Article  Google Scholar 

  • García, C., Bravo, M. C., Lagos, M., and Lagos, N., 2004. Paralytic shellfish poisoning: Post mortem analysis of tissue and body fluid samples from human victims in the patagonia fjords. Toxicon, 43: 149–158.

    Article  Google Scholar 

  • Gubbins, M. J., Eddy, F. B., Gallacher, S., and Stagg, R. M., 2000. Paralytic shellfish poisoning toxins induce xenobiotic metabolishing enzymes in Atlantic salmon (Salmo salar). Marine Environmental Research, 50: 479–483.

    Article  Google Scholar 

  • Jeon, J. K., Lee, J. S., Shim, W. J., Aarakawa, O., Takatani, T., Honda, S., and Noguchi, T., 2008. Changes in activity of hepatic xenobiotic-metabolizing enzymes of tiger puffer (Takifugu rubripes) exposed to paralytic shellfish poisoning toxins. Journal of Environmental Biology, 29: 599–603.

    Google Scholar 

  • Leu, J. H., Wang, H. C., Kou, G. H., and Lo, C. F., 2008. Penaeus monodon caspase is targeted by a white spot syndrome virus anti-apoptosis protein. Developmental and Comparative Immunology, 32: 476–486.

    Article  Google Scholar 

  • Li, Y. Q., Li, J., and Wang, Q. Y., 2006. The effects of dissolved oxygen concentration and stocking density on growth and non-specific immunity factors in Chinese shrimp, Fennero-penaeus chinensis. Aquaculture, 256: 608–616.

    Article  Google Scholar 

  • Lin, Y. S., 1996. Red tide caused by a marine toxic dinoflagellate, Alexandrium tamarensis (Lebour) Baleon, in shrimp ponds in Xiamen. Taiwan Strait, 15: 16–18 (in Chinese).

    Google Scholar 

  • Livingstone, D. R., 2001. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin, 42: 656–666.

    Article  Google Scholar 

  • Livingstone, D. R., 2003. Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Revue De Medecine Veterinaire, 154: 427–430.

    Google Scholar 

  • Marisa, L. W., and Juan, F. M., 2005. Real-time PCR for mRNA quantitation. Biotechniques, 39: 75–85.

    Article  Google Scholar 

  • Ron, V. D. O., Jonny, B., and Nico, P. E. V., 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environmental Toxicology and Pharmacology, 13: 57–149.

    Article  Google Scholar 

  • Sakamoto, S., Sato, S., Ogata, T., and Kodama, M., 2000. Formation of intermediate conjugates in the reductive transformation of gonyautoxins to saxitoxins by thiolcompounds. Fisheries Science, 66: 136–141.

    Article  Google Scholar 

  • Sato, S., Sakai, R., and Kodama, M., 2000. Identification of thioether intermediates in the reductive transformation of gonyautoxins into saxitoxins by thiols. Bioorganic & Medicinal Chemistry Letters, 10: 1787–1789.

    Article  Google Scholar 

  • Skulachev, V. P., 1998. Cytochromec in the apoptotic and antioxidant cascades. Febs Letters, 423: 275–280.

    Article  Google Scholar 

  • Stephan, P., Claudia, W., Stephanie, W., Helge, S., and Harri, K., 2005. Activity and substrate specificity of cytosolic and microsomal glutathione S-transferase in Australian black tiger prawns (Penaeus monodon) after exposure to cyanobacterial toxins. Environmental Toxicology, 20: 301–307.

    Article  Google Scholar 

  • Su, H. M., Liao, I. C., and Chiang, Y. M., 1993. Mass mortality of prawn caused by Alexandrium tamarense blooming in a culture pond in southern Taiwan. In: Toxic Phytoplankton Blooms in the Sea. Smayda, T. J., and Shimizu, Y., eds., Elsevier Science Publishers B V, Amsterdam, 329–333.

    Google Scholar 

  • Tan, Z. J., Yan, T., Zhou, M. J., Li, J., Yu, R. C., and Wang, Y. F., 2002. The effects of Alexandrium tamarense on survival, growth and reproduction of Neomysis awatschensis. Acta Ecologica Sinica, 22: 1635–1639.

    Google Scholar 

  • Sun, Y., Yin, G., Zhang, J., Yu, H., and Wang, X., 2007. Bioaccumulation and ROS generation in liver of freshwater fish, goldfish Carassius auratus under HC Orange No.1 exposure. Environmental Toxicology, 22: 256–263.

    Article  Google Scholar 

  • Tan, Z. J., 2006. Toxic effects and its mechanism of dinoflagellate Alexandrium tamarense on perch Lateolabrax japonicus. Ph.D thesis. Chinese Academy of Sciences, 24–34.

    Google Scholar 

  • Tan, Z. J., Yan, T., and Yu, R. C., 2007. Transfer of paralytic shellfish toxins via marine food chains: A simulated experiment. Biomedical and Environmental Sciences, 20: 235–241.

    Google Scholar 

  • Thornberry, N. A., 1998. Caspases: Key mediators of apoptosis. Chemistry and Biology, 5: 97–103.

    Article  Google Scholar 

  • Trezado, C., Hidalgo, M. C., García-Gallego, M., Morales, A. E., Furne, M., Domezain, A., Domezain, J., and Sanz, A., 2006. Antioxidant enzymes and lipid peroxidation in sturgeon Acipenser naccarii and trout Oncorhynchus mykiss. A comparative study. Aquaculture, 254: 758–767.

    Article  Google Scholar 

  • Wang, W., and Ballatori, N., 1998. Endogenous glutathione conjugates: Occurrence and biological functions. Pharmacological Reviews, 50: 335–352.

    Google Scholar 

  • Wang, Y., Li, J., Liu, P., Li, J. T., Zhang, Z., Chang, Z. Q., He, Y. Y., and Liu, D. Y., 2011. The responsive expression of a caspase gene in Chinese shrimp Fenneropenaeus chinensis against pH stress. Aquaculture Research, 42: 1214–1230.

    Article  Google Scholar 

  • Winston, G. W., 1991. Oxidants and antioxidants in aquatic animals. Comparative Biochemistry and Physiology Part C Comparative Pharmacology, 100: 173–176.

    Article  Google Scholar 

  • Xu, W. N., Liu, W. B., and Liu, Z. P., 2009. Trichlorfon-induced apoptosis in hepatocyte primary cultures of Carassius auratus gibelio. Chemosphere, 77: 895–901.

    Article  Google Scholar 

  • Yan, T., Zhou, M. J., Fu, M., Yu, R. C., Wang, Y. F., and Li, J., 2003. Effects of the dinoflagellate Alexandrium tamarense on early development of the Scallop Argopectan irradians concentricus. Aquaculture, 217: 167–178.

    Article  Google Scholar 

  • Zhu, M. Y., 1993. Red tide in shrimp ponds along the Bohai Sea. In: Toxic Phytoplankton Blooms in the Sea. Smayda, T. J., and Shimizu, Y., eds., Elsevier Science Publishers B V, Amsterdam, 363–367.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, P.R. China

    Zhongxiu Liang & Hai Ren

  2. Key Laboratory of Sustainable Development of Marine Fisheries of Ministry of Agriculture; Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, P. R. China

    Zhongxiu Liang, Jian Li, Jitao Li, Zhijun Tan & Fazhen Zhao

Authors
  1. Zhongxiu Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jitao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhijun Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hai Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fazhen Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liang, Z., Li, J., Li, J. et al. Toxic dinoflagellate Alexandrium tamarense induces oxidative stress and apoptosis in hepatopancreas of shrimp (Fenneropenaeus chinensis). J. Ocean Univ. China 13, 1005–1011 (2014). https://doi.org/10.1007/s11802-014-2397-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-014-2397-8

Key words

Search

Navigation