Skip to main content
Log in

Regulation of metallothionein gene expression in response to benzo[a]pyrene exposure and bacterial challenge in marine cultured black porgy (Acanthopagrus schlegelii)

  • Published:
Chinese Journal of Geochemistry Aims and scope Submit manuscript

Abstract

Metallothioneins (MTs) are normally considered to be sensitive indicators of heavy metal pollution, but it is less clear whether the MT gene can actively respond to other environmental stresses. In this study, an MT mRNA molecular sequence of 471 bp (full length) was identified in marine cultured black porgy (Acanthopagrus schlegelii), encoding 60 amino acids containing 20 cysteine residues. The MT sequence was highly homologous to that of other fish belonging to the MT superfamily type 1 family. The three dimensional structure of the deduced MT peptide was composed of two metal-binding domains capable of ligating divalent heavy metals. The MT mRNA transcripts were detected in the 11 tested tissues and the highest quantity was present in the liver. Stresses by two factors, benzo[a]pyrene (B[a]p) exposure and bacterial challenge, were evaluated on MT gene expression. The level of MT gene transcripts in the liver significantly declined 24 h post B[a]p exposure and the quantity was significantly correlated with the exposure time during a 24 h period. In contrast, MT gene expression in the liver was significantly increased 48 h post bacterial infection and the quantity was significantly correlated with the infection time during this period of 48 h. Our results indicated that MT gene expression in black porgy liver was sensitive to environmental stresses other than just the heavy metal pollution reported, suggesting that the development of a reliable biomarker for heavy metal pollution will be more complex than expected.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Amiard J.C., Amiard-Triquet C., Barka S., Pellerin J., and Rainbow P.S. (2006) Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers [J]. Aquatic Toxicology. 76, 160–202.

    Article  Google Scholar 

  • Arnold K., Bordoli L., Kopp J., and Schwede T. (2006) The SWISS-MODEL Workspace: A web-based environment for protein structure homology modelling [J]. Bioinformatics. 22, 195–201.

    Article  Google Scholar 

  • Braun W., Vasák M., Robbins A.H., Stout C.D., Wagner G., Kägi J.H.R., and Wüthrich K. (1992) Comparison of the NMR solution structure and the X-ray crystal structure of rat metallo-thionein-2 [J]. Proceedings of the National Academy of Sciences of the United States of America. 89, 10124–10128.

    Article  Google Scholar 

  • Burczynski M.E., Lin H.K., and Penning T.M. (1999) Isoform-specific induction of a human aldo-keto reductase by polycyclic aromatic hydrocarbons (PAHs), electrophiles, and oxidative stress: Implications for the alternative pathway of PAH activation catalyzed by human dihydrodiol dehydrogenase [J]. Cancer Research. 59, 607–614.

    Google Scholar 

  • Capasso C., Carginale V., Crescenzi O., Maro D.D., Parisi E., Spadaccini R., and Temussi P.A. (2003) Solution structure of MT_nc, a novel metallothionein from the Antarctic fish Notothenia coriiceps [J]. Structure. 11, 435–443.

    Article  Google Scholar 

  • Cho Y.S., Lee S.Y., Kim K.Y., Bang I.C., Kim D.S., and Nam Y.K. (2008) Gene structure and expression of metallothionein during metal exposures in Hemibarbus mylodon [J]. Ecotoxicology and Environmental Safety. 71, 125–137.

    Article  Google Scholar 

  • Creti P., Trinchella F., and Scudiero R. (2010) Heavy metal bioaccumulation and metallothionein content in tissues of the sea bream Sparus aurata from three different fish farming systems [J]. Environmental Monitoring and Assessment. 165, 321–329.

    Article  Google Scholar 

  • Inoue K., Takano H., Shimada A., and Satoh M. (2009) Metallothionein as an anti-inflammatory mediator [J]. Mediators of Inflammation. 101, 659–665.

    Google Scholar 

  • Jenny M.J., Warr G.W., Ringwood A.H., Baltzegar D.A., and Chapman R.W. (2006) Regulation of metallothionein genes in the American oyster (Crassostrea virginica): Ontogeny and differential expression in response to different stressors [J]. Gene. 379, 156–165.

    Article  Google Scholar 

  • Kim K.B. and Lee B.M. (1997) Oxidative stress to DNA, protein, and antioxidant enzymes (superoxide dismutase and catalase) in rats treated with benzo(a)pyrene [J]. Cancer Letters. 113, 205–212.

    Article  Google Scholar 

  • Klaassen C.D., Liu J., and Diwan B.A. (2009) Metallothionein protection of cadmium toxicity [J]. Toxicology and Applied Pharmacology. 238, 215–220.

    Article  Google Scholar 

  • Kling P. and Olsson P.E. (2005) Metallothionein: Structure and regulation. In Biochemistry and Molecular Biology (eds. Mommsen T.P. and Moon T.W.) [M]. pp.289–302. Elsevier, Amsterdam.

    Google Scholar 

  • Ladhar-Chaabouni R, Machreki-Ajmi M, and Hamza-Chaffai A. (2012) Use of metallothioneins as biomarkers for environmental quality assessment in the Gulf of Gabès (Tunisia) [J]. Environmental Monitoring and Assessment. 184, 2177–2192.

    Article  Google Scholar 

  • Li Qingzhao, Zhang Xian, and Yan Changzhou (2010) Polycyclic aromatic hydrocarbon contamination of recent sediments and marine organisms from Xiamen Bay, China [J]. Archives of Environmental Contamination and Toxicology. 58, 711–721.

    Article  Google Scholar 

  • Ma Qiang (2010) Transcriptional responses to oxidative stress: Pathological and toxicological implications [J]. Pharmacology & Therapeutics. 125, 376–393.

    Article  Google Scholar 

  • Margoshes M. and Vallee B.L. (1957) A cadmium protein from equine kidney cortex [J]. Journal of the American Chemical Society. 79, 1813–1814.

    Article  Google Scholar 

  • Paul-Pont I., Gonzalez P., Baudrimont M., Nili H., and de Montaudouin X. (2010) Short-term metallothionein inductions in the edible cockle Cerastoderma edule after cadmium or mercury exposure: Discrepancy between mRNA and protein responses [J]. Aquatic Toxicology. 97, 260–267.

    Article  Google Scholar 

  • Tian Yun, Luo Yuanrong, Zheng Tianling, Cai Lizhe, Cao Xiaoxing, and Yan Chongling (2008) Contamination and potential biodegradation of polycyclic aromatic hydrocarbons in mangrove sediments of Xiamen, China [J]. Marine Pollution Bulletin. 56, 1184–1191.

    Article  Google Scholar 

  • Tsuji G., Takahara M., Uchi H., Takeuchi S., Mitoma C., Moroi Y., and Furue M. (2011) An environmental contaminant, benzo(a)pyrene, induces oxidative stress-mediated interleukin-8 production in human keratinocytes via the aryl hydrocarbon receptor signaling pathway [J]. Journal of Dermatological Science. 62, 42–49.

    Google Scholar 

  • Van den Hurk P., Faisal M., and Roberts Jr M.H. (2000) Interactive effects of cadmium and benzo[a]pyrene on metallothionein induction in mummichog (Fundulus heteroclitus) [J]. Marine Environmental Research. 50, 83–87.

    Article  Google Scholar 

  • Wang Kejian, Bo Jun, Yang Ming, Hong Huasheng, Wang Xinhong, Chen Fangyi, and Yuan Jianjun (2009) Hepcidin gene expression induced in the developmental stages of fish upon exposure to benzo[a]pyrene (Bap) [J]. Marine Environmental Research. 67, 159–165.

    Article  Google Scholar 

  • Yang Ming, Chen Bei, Cai Jingjing, Peng Hui, Cai Ling, Yuan Jianjun, and Wang Kejian (2011) Molecular characterization of hepcidin AS-hepc2 and AS-hepc6 in black porgy (Acanthopagrus schlegelii): Expression pattern responded to bacterial challenge and in vitro antimicrobial activity [J]. Comparative Biochemistry and Physiology B—Biochemistry & molecular Biology. 158, 155–163.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ming Yang or Kejian Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, M., Pan, C., Bo, J. et al. Regulation of metallothionein gene expression in response to benzo[a]pyrene exposure and bacterial challenge in marine cultured black porgy (Acanthopagrus schlegelii). Chin. J. Geochem. 33, 404–410 (2014). https://doi.org/10.1007/s11631-014-0705-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11631-014-0705-z

Key words

Navigation