Skip to main content
SpringerLink
Log in

Identification of protein biomarkers of mercury toxicity in fish

  • Original Paper
  • Published:
Environmental Chemistry Letters Aims and scope Submit manuscript

Abstract

Bioaccumulative metals such as mercury are found in increasing amounts in fish and their consumers. In the region of the Madeira River, in the Brazilian Amazon, mercury (Hg) is a predominant contaminant in the aquatic ecosystem. There is therefore a need to find specific biomarkers of mercury toxicity in fish to monitor contaminations. Here, mercury-bound proteins were identified in the liver tissues of fishes Mylossoma duriventre and Brachyplatystoma rousseauxii. Mercury was quantified in liver tissue, pellets and protein spots by graphite furnace atomic absorption. Proteins were fractionated by two-dimensional polyacrylamide gel electrophoresis and identified by mass spectrometry with electrospray ionization. We identified nine proteins linked to mercury and that presented biomarker characteristics of mercury. Among the proteins identified, isoforms of parvalbumin, ubiquitin-40S ribosomal protein S27a, brain-specific angiogenesis inhibitor 1-associated protein 2-like protein 2 and betaine–homocysteine S-methyltransferase 1 are notable for having the molecular function of binding to metallic ions.

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

Similar content being viewed by others

References

  • Avramescu ML, Yumvihoze E, Hintelmann H et al (2011) Biogeochemical factors influencing net mercury methylation in contaminated freshwater sediments from the St. Lawrence River in Cornwall, Ontario, Canada. Sci Total Environ 409:968–978. doi:10.1016/j.scitotenv.2010.11.016

    Article  CAS  Google Scholar 

  • Braga CP, Bittarello AC, Padilha CCF et al (2015) Mercury fractionation in dourada (Brachyplatystoma rousseauxii) of the Madeira River in Brazil using metalloproteomic strategies. Talanta 132:239–244. doi:10.1016/j.talanta.2014.09.021

    Article  CAS  Google Scholar 

  • Carvalho ME, Gasparin G, Poleti MD et al (2014) Heat shock and structural proteins associated with meat tenderness in Nellore beef cattle, a Bos indicus breed. Meat Sci 96:1318–1324. doi:10.1016/j.meatsci.2013.11.014

    Article  CAS  Google Scholar 

  • Chmurzyńska A (2006) The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. J Appl Genet 47:39–48. doi:10.1007/BF03194597

    Article  Google Scholar 

  • Freidl R, Gstoettner A, Baranyi U et al (2016) Blocking antibodies induced by immunization with a hypoallergenic parvalbumin mutant reduce allergic symptoms in a mouse model of fish allergy. J Allergy Clin Immunol. doi:10.1016/j.jaci.2016.10.018

    Google Scholar 

  • Garcia JS, De Magalhães CS, Arruda MAZ (2006) Trends in metal-binding and metalloprotein analysis. Talanta 69:1–15. doi:10.1016/j.talanta.2005.08.041

    Article  CAS  Google Scholar 

  • González B, Pajares MA, Martínez-Ripoll M et al (2004) Crystal structure of rat liver betaine homocysteine s-methyltransferase reveals new oligomerization features and conformational changes upon substrate binding. J Mol Biol 338:771–782. doi:10.1016/j.jmb.2004.03.005

    Article  Google Scholar 

  • González-Estecha M, Bodas-Pinedo A, Guillén-Pérez JJ et al (2014) Methylmercury exposure in the general population; toxicokinetics; differences by gender, nutritional and genetic factors. Nutr Hosp 30:969–988. doi:10.3305/nh.2014.30.5.7727

    Google Scholar 

  • Heinrich PC, Behrmann I, Müller-Newen G, Schaper F GL (1998) Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. - PubMed - NCBI. http://www.ncbi.nlm.nih.gov/pubmed/9716487

  • Hellal J, Guédron S, Huguet L et al (2015) Mercury mobilization and speciation linked to bacterial iron oxide and sulfate reduction: a column study to mimic reactive transfer in an anoxic aquifer. J Contam Hydrol 180:56–68. doi:10.1016/j.jconhyd.2015.08.001

    Article  CAS  Google Scholar 

  • Hsu E (1994) The variation in immunoglobulin heavy chain constant regions in evolution. Semin Immunol 6:383–391. doi:10.1006/smim.1994.1048

    Article  CAS  Google Scholar 

  • Inácio AF (2006) Metalotioneína e Metais em Geophagus brasiliensis - Acará. 78

  • Karsi A, Patterson A, Feng J, Liu Z (2002) Translational machinery of channel catfish: I. A transcriptomic approach to the analysis of 32 40S ribosomal protein genes and their expression. Gene 291:177–186

    Article  CAS  Google Scholar 

  • Kim YJ, Björklund S, Li Y et al (1994) A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell 77:599–608

    Article  CAS  Google Scholar 

  • Lee Y, Lee DH, Kho CW et al (2005) Transthyretin-related proteins function to facilitate the hydrolysis of 5-hydroxyisourate, the end product of the uricase reaction. FEBS Lett 579:4769–4774. doi:10.1016/j.febslet.2005.07.056

    Article  CAS  Google Scholar 

  • Macirella R, Guardia A, Pellegrino D et al (2016) effects of two sublethal concentrations of mercury chloride on the morphology and metallothionein activity in the liver of Zebrafish (Danio rerio). Int J Mol Sci 17:1–16. doi:10.3390/ijms17030361

    Article  Google Scholar 

  • Moraes PM, Santos FA, Padilha CCF et al (2012) A preliminary and qualitative metallomics study of mercury in the muscle of fish from Amazonas, Brazil. Biol Trace Elem Res 150:195–199. doi:10.1007/s12011-012-9502-x

    Article  Google Scholar 

  • Moraes PM, Santos FA, Cavecci B et al (2013) GFAAS determination of mercury in muscle samples of fish from Amazon, Brazil. Food Chem 141:2614–2617. doi:10.1016/j.foodchem.2013.05.008

    Article  CAS  Google Scholar 

  • Pearson RG (1963) Hard and soft acids and bases. J Am Chem Soc 85:3533–3539. doi:10.1021/ja00905a001

    Article  CAS  Google Scholar 

  • Perrot V, Bridou R, Pedrero Z et al (2015) Identical Hg isotope mass dependent fractionation signature during methylation by sulfate-reducing bacteria in sulfate and sulfate-free environment. Environ Sci Technol 49:1365–1373. doi:10.1021/es5033376

    Article  CAS  Google Scholar 

  • Queiroz LJ, Vilara-Torrente G, Ohara WM, Pires THS, Zuanon J, Doria CRC (2013) Peixes do Rio Madeira, 1º ed., Brazilian Chamber of Books, São Paulo-Brazil

  • Queiroz LJ, Vilara-Torrente G, Ohara WM, Pires THS, Zuanon J, Doria CRC (2014) Peixes do Rio Madeira. São Paulo

  • Rivera SJ, Pacheco LF, Acha D et al (2016) Low total mercury in Caiman yacare (Alligatoridae) as compared to carnivorous, and non-carnivorous fish consumed by Amazonian indigenous communities. Environ Pollut 218:366–371. doi:10.1016/j.envpol.2016.07.013

    Article  CAS  Google Scholar 

  • Scita G, Confalonieri S, Lappalainen P, Suetsugu S (2008) IRSp53: crossing the road of membrane and actin dynamics in the formation of membrane protrusions. Trends Cell Biol 18:52–60. doi:10.1016/j.tcb.2007.12.002

    Article  CAS  Google Scholar 

  • Senger MR, Rosemberg DB, Seibt KJ et al (2010) Influence of mercury chloride on adenosine deaminase activity and gene expression in zebrafish (Danio rerio) brain. Neurotoxicology 31:291–296. doi:10.1016/j.neuro.2010.03.003

    Article  CAS  Google Scholar 

  • Tenório-Daussat CL, Resende MCM, Ziolli RL et al (2014) Evaluation and standardization of different purification procedures for fish bile and liver metallothionein quantification by spectrophotometry and SDS-PAGE analyses. Talanta 120:491–497. doi:10.1016/j.talanta.2013.11.070

    Article  Google Scholar 

  • UniProt (2016) Universal Protein Resource (UniProt). In: 2016. http://www.uniprot.org/. Accessed 28 Apr 2016

  • UniProt Consortium (2016) rps27a—Ubiquitin-40S ribosomal protein S27a precursor—Ictalurus punctatus (Channel catfish)—rps27a gene & protein. In: 2002-2016. http://www.uniprot.org/uniprot/P68200. Accessed 11 Apr 2016

  • Van Gestel CA, Van Brummelen TC (1996) Incorporation of the biomarker concept in ecotoxicology calls for a redefinition of terms. Ecotoxicology 5:217–225. doi:10.1007/BF00118992

    Article  Google Scholar 

  • Vieira JCS, Cavecci B, Queiroz JV et al (2015) Determination of the mercury fraction linked to protein of muscle and liver tissue of Tucunaré (Cichla spp.) from the Amazon Region of Brazil. Arch Environ Contam Toxicol 69:422–430. doi:10.1007/s00244-015-0160-9

    Article  CAS  Google Scholar 

  • Wallace MAG, Kormos TM, Pleil JD (2016) Blood-borne biomarkers and bioindicators for linking exposure to health effects in environmental health science. J Toxicol Environ Heal Part B 19:380–409. doi:10.1080/10937404.2016.1215772

    Article  CAS  Google Scholar 

  • Weiss EP, Brown MD, Shuldiner AR, Hagberg JM (2002) Fatty acid binding protein-2 gene variants and insulin resistance: gene and gene-environment interaction effects. Physiol Genomics 10:145–157. doi:10.1152/physiolgenomics.00070.2001

    Article  CAS  Google Scholar 

  • Wiklund JA, Kirk JL, Muir DCG et al (2017) Anthropogenic mercury deposition in Flin Flon Manitoba and the Experimental Lakes Area Ontario (Canada): a multi-lake sediment core reconstruction. Sci Total Environ 586:685–695. doi:10.1016/j.scitotenv.2017.02.046

    Article  CAS  Google Scholar 

  • Zeng L, Luo G, He T et al (2016) Effects of sulfate-reducing bacteria on methylmercury at the sediment–water interface. J Environ Sci 46:214–219. doi:10.1016/j.jes.2016.05.018

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the Brazilian research funding agencies FAPESP (processes 2013/21297-1 and 2014/02668-1) and ANEEL/ESBR (P&D: 6631-0001/2012/Contract Jirau 004/201) for their financial support.

Author information

Authors and Affiliations

  1. Institute of Biosciences, São Paulo State University (UNESP), Botucatu, 18618-970, Brazil

    José Cavalcante Souza Vieira, Grasieli de Oliveira, Bruna Cavecci & Pedro de Magalhães Padilha

  2. University of Nebraska-Lincoln, Lincoln, NE, USA

    Camila Pereira Braga

  3. School of Veterinary Medicine and Animal Science, São Paulo State University (UNESP), Botucatu, Brazil

    João Vitor de Queiroz & Alis Correia Bittarello

  4. University of São Paulo (USP), Bauru, Brazil

    Aline de Lima Leite & Marília Afonso Rabelo Buzalaf

  5. College of Planaltina, University of Brasília (UnB), Federal District, Brazil

    Luiz Fabricio Zara

Authors
  1. José Cavalcante Souza Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camila Pereira Braga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Grasieli de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aline de Lima Leite
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. João Vitor de Queiroz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bruna Cavecci
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alis Correia Bittarello
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marília Afonso Rabelo Buzalaf
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Luiz Fabricio Zara
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Pedro de Magalhães Padilha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José Cavalcante Souza Vieira.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vieira, J.C.S., Braga, C.P., de Oliveira, G. et al. Identification of protein biomarkers of mercury toxicity in fish. Environ Chem Lett 15, 717–724 (2017). https://doi.org/10.1007/s10311-017-0644-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10311-017-0644-0

Keywords

Search

Navigation