Advertisement

Biological Trace Element Research

, Volume 187, Issue 1, pp 291–300 | Cite as

Identification of Biomarkers of Mercury Contamination in Brachyplatystoma filamentosum of the Madeira River, Brazil, Using Metalloproteomic Strategies

  • João Vitor de Queiroz
  • José Cavalcante Souza VieiraEmail author
  • Grasieli de Oliveira
  • Camila Pereira Braga
  • Izabela da Cunha Bataglioli
  • Janaína Macedo da Silva
  • Wellington Luiz de Paula Araújo
  • Pedro de Magalhães Padilha
Article

Abstract

Predator fish can accumulate high levels of mercury, which qualifies them as potential indicators of this toxic metal. The predatory species Brachyplatystoma filamentosum, popularly known as filhote, is among the most consumed species in the Brazilian Amazon. Continuing the metalloproteomic studies of mercury in Amazonian fishes that have been developed in the last 5 years, the present paper provides the data of protein characterization associated with mercury in muscle and liver samples of filhote (Brachyplatystoma filamentosum) collected in the Madeira River, Brazilian Amazon. The mercury concentration in the muscle and liver samples was determined by graphite furnace atomic absorption spectrometry (GFAAS). The protein fraction was extracted in an aqueous medium, and later, a fractional precipitation procedure was performed to obtain the protein pellets. Then, the proteome of the tissue samples of this fish species was separated by two-dimensional polyacrylamide gel electrophoresis (2D-PAGE), and a mercury mapping of the protein spots was carried out by GFAAS after acid digestion. Protein spots that had mercury were characterized by mass spectrometry with electrospray ionization in sequence (ESI-MS/MS) after tryptic digestion. It was possible to characterize 11 mercury-associated protein spots that presented biomarker characteristics and could be used to monitor mercury in fish species of the Amazon region. Thus, the metalloproteomic strategies used in the present study allowed us to characterize 11 mercury-associated protein spots. It should be noted that the protein spots identified as GFRP, TMEM186, TMEM57B, and BHMT, which have coordination sites for elements with characteristics of soft acids, such as mercury, can be used as biomarkers of mercury contamination in monitoring studies of this toxic metal in fish species from the Amazon region.

Keywords

Biomarkers Proteomics System biology Mercury Proteins 

Notes

Funding Information

The authors thank the Brazilian research funding agency ANEEL/ESBR-P&D: 6631-0001/2012/Contract Jirau 004/2013, São Paulo State Research Foundation-FAPESP (Processes:2010/51332-5, 2013/21297-1 and 2016/19404-2), National Council for Scientific and Technological Development–CNPq (Process: 303719/2014-1), and Coordination for the Improvement of Higher Education Personnel-CAPES for their financial support.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interest.

References

  1. 1.
    Moraes PM, Santos FA, Cavecci B, Padilha CCF, Vieira JCS, Roldan PS, Padilha PM (2013) GFAAS determination of mercury in muscle samples of fish from Amazon, Brazil. Food Chem 141:2614–2617.  https://doi.org/10.1016/j.foodchem.2013.05.008 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Braga CP, Bittarello a C, Padilha CCF et al (2015) Mercury fractionation in dourada (Brachyplatystoma rousseauxii) of the Madeira River in Brazil using metalloproteomic strategies. Talanta 132:239–244.  https://doi.org/10.1016/j.talanta.2014.09.021 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Vieira JCS, Braga CP, de Oliveira G, do Carmo Federici Padilha C, de Moraes PM, Zara LF, de Lima Leite A, Buzalaf MAR, de Magalhães Padilha P (2017) Correction to: mercury exposure: protein biomarkers of mercury exposure in Jaraqui fish from the Amazon region. Biol Trace Elem Res 183(1):172.  https://doi.org/10.1007/s12011-017-1195-8 CrossRefGoogle Scholar
  4. 4.
    Vieira JCS, Cavecci B, Queiroz JV, Braga CP, Padilha CCF, Leite AL, Figueiredo WS, Buzalaf MAR, Zara LF, Padilha PM (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.  https://doi.org/10.1007/s00244-015-0160-9 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Silva FA, Cavecci B, Baldassini WA, Lima PM, Moraes PM, Roldan PS, Padilha CCF, Padilha PM (2013) Selenium fractionation from plasma, muscle and liver of Nile tilapia (Oreochromis niloticus). J Food Meas Charact 7:158–165CrossRefGoogle Scholar
  6. 6.
    dos Santos FA, Lima PM, Neves RCF et al (2011) Metallomic study on plasma samples from Nile tilapia using SR-XRF and GFAAS after separation by 2D PAGE: initial results. Microchim Acta 173:43–49.  https://doi.org/10.1007/s00604-010-0522-y CrossRefGoogle Scholar
  7. 7.
    Lima PM, Neves RDCF, dos Santos FA et al (2010) Analytical approach to the metallomic of Nile tilapia (Oreochromis niloticus) liver tissue by SRXRF and FAAS after 2D-PAGE separation: preliminary results. Talanta 82:1052–1056.  https://doi.org/10.1016/j.talanta.2010.06.023 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Garcia JS, De Magalhães CS, Arruda MAZ (2006) Trends in metal-binding and metalloprotein analysis. Talanta 69:1–15.  https://doi.org/10.1016/j.talanta.2005.08.041 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Cavalcante J, Vieira S, Braga CP et al (2017) Mercury exposure: protein biomarkers of mercury exposure in Jaraqui fish from the Amazon region. Biol Trace Elem Res 183:164–171.  https://doi.org/10.1007/s12011-017-1129-5 CrossRefGoogle Scholar
  10. 10.
    Shevchenko A, Tomas H, Havlis J et al (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856–2860.  https://doi.org/10.1038/nprot.2006.468 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Moraes PM, Santos FA, Padilha CCF, Vieira JCS, Zara LF, de M. Padilha P (2012) A preliminary and qualitative metallomics study of mercury in the muscle of fish from Amazonas, Brazil. Biol Trace Elem Res 150:195–199.  https://doi.org/10.1007/s12011-012-9502-x CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Neves RCF, Lima PM, De Medicina F et al (2012) Artigo 35:493–498Google Scholar
  13. 13.
    Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832–619812.  https://doi.org/10.1155/2008/619832 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Sharp MF, Lopata AL (2014) Fish allergy: in review. Clin Rev Allergy Immunol 46:258–271.  https://doi.org/10.1007/s12016-013-8363-1 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Kobayashi A, Tanaka H, Hamada Y, Ishizaki S, Nagashima Y, Shiomi K (2006) Comparison of allergenicity and allergens between fish white and dark muscles. Allergy: European. J Allergy Clin Immunol 61:357–363.  https://doi.org/10.1111/j.1398-9995.2006.00966.x CrossRefGoogle Scholar
  16. 16.
    Arif SH (2009) A Ca2+-binding protein with numerous roles and uses: parvalbumin in molecular biology and physiology. BioEssays 31:410–421.  https://doi.org/10.1002/bies.200800170 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Schwaller B (2009) The continuing disappearance of “pure” Ca2+ buffers. Cell Mol Life Sci 66:275–300.  https://doi.org/10.1007/s00018-008-8564-6 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Li L, Rezvan A, Salerno JC, Husain A, Kwon K, Jo H, Harrison DG, Chen W (2010) GTP cyclohydrolase i phosphorylation and interaction with GTP cyclohydrolase feedback regulatory protein provide novel regulation of endothelial tetrahydrobiopterin and nitric oxide. Circ Res 106:328–336.  https://doi.org/10.1161/CIRCRESAHA.109.210658 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Ichinose H, Ohye T, Matsuda Y, Hori TA, Blau N, Burlina A, Rouse B, Matalon R, Fujita K, Nagatsu T (1995) Characterization of mouse and human GTP cyclohydrolase I genes: mutations in patients with GTP cyclohydrolase I deficiency. J Biol Chem 270:10062–10071CrossRefGoogle Scholar
  20. 20.
    Maita N, Okada K, Hatakeyama K, Hakoshima T (2002) Crystal structure of the stimulatory complex of GTP cyclohydrolase I and its feedback regulatory protein GFRP. Proc Natl Acad Sci U S A 99:1212–1217.  https://doi.org/10.1073/pnas.022646999 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    de Brevern AG (2010) 3D structural models of transmembrane proteins. Methods Mol Biol 654:387–401.  https://doi.org/10.1007/978-1-60761-762-4_20 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    von Heijne G (1994) Membrane proteins: from sequence to structure. Annu Rev Biophys Biomol Struct 23:167–192.  https://doi.org/10.1146/annurev.bb.23.060194.001123 CrossRefGoogle Scholar
  23. 23.
    Mattjus P (2009) Glycolipid transfer proteins and membrane interaction. Biochim Biophys Acta 1788:267–272.  https://doi.org/10.1016/j.bbamem.2008.10.003 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Abe A, Sasaki T (1989) Formation of an intramolecular disulfide bond of glycolipid transfer protein. BBA-Biomembranes 985:45–50.  https://doi.org/10.1016/0005-2736(89)90101-6 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Abe A, Sasaki T (1989) Sulfhydryl groups in glycolipid transfer protein: formation of an intramolecular disulfide bond and oligomers by Cu2+-catalyzed oxidation. BBA-Biomembranes 985:38–44.  https://doi.org/10.1016/0005-2736(89)90100-4 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Ratnam S, Wijekoon EP, Hall B, Garrow TA, Brosnan ME, Brosnan JT (2006) Effects of diabetes and insulin on betaine-homocysteine S-methyltransferase expression in rat liver. Am J Phys Endocrinol Metab 290:E933–E939.  https://doi.org/10.1152/ajpendo.00498.2005 CrossRefGoogle Scholar
  27. 27.
    Vlieghe P, Lisowski V, Martinez J, Khrestchatisky M (2010) Synthetic therapeutic peptides: science and market. Drug Discov Today 15:40–56.  https://doi.org/10.1016/j.drudis.2009.10.009 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • João Vitor de Queiroz
    • 1
  • José Cavalcante Souza Vieira
    • 2
    Email author
  • Grasieli de Oliveira
    • 2
  • Camila Pereira Braga
    • 3
  • Izabela da Cunha Bataglioli
    • 1
  • Janaína Macedo da Silva
    • 2
  • Wellington Luiz de Paula Araújo
    • 1
  • Pedro de Magalhães Padilha
    • 1
    • 2
  1. 1.School of Veterinary Medicine and Animal ScienceSão Paulo State University (UNESP)BotucatuBrazil
  2. 2.Institute of BiosciencesSão Paulo State University (UNESP)BotucatuBrazil
  3. 3.Biochemistry DepartmentUniversity of NebraskaLincolnUSA

Personalised recommendations