Abstract
Recent studies have demonstrated the association of mercury (Hg) with some fish proteins, milk, and hair from individuals exposed to the element in the Amazon. However, few studies involve identifying biomarkers of mercury exposure. Therefore, the present study aimed to identify potential biomarkers of Hg exposure in fish. For this, the muscular tissues of two species of fish (Prochilodus lineatus and Mylossoma duriventre) that feed the Amazonian human population were analyzed. Through the analyses obtained by graphite furnace atomic absorption spectrometry (GFAAS), it was possible to identify four protein SPOTS where mercury was present. These SPOTS, identified by mass spectrometry (ESI-MS/MS), included parvalbumin and ubiquitin-40S ribosomal protein S27a, and these being metalloproteins with biomarker characteristics. In addition, the results show the intense Hg/protein ratio observed in the two proteins, which makes metalloproteins strong candidates for biomarkers of mercury exposure.
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References
Berky AJ, Ryde IT, Feingold B et al (2018) Predictors of mitochondrial DNA copy number and damage in a mercury-exposed rural Peruvian population near artisanal and small-scale gold mining: an exploratory study. Environ Mol Mutagen. https://doi.org/10.1002/em.22244
Hacon S, Barrocas PRG, de Vasconcellos ACS et al (2008) An overview of mercury contamination research in the Amazon basin with an emphasis on Brazil. Cad saúde pública 24:1479–1492
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. https://doi.org/10.1016/j.foodchem.2013.05.008
Passos CJS, Da Silva DS, Lemire M et al (2008) Daily mercury intake in fish-eating populations in the Brazilian Amazon. J Expo Sci Environ Epidemiol 18:76–87. https://doi.org/10.1038/sj.jes.7500599
Bravo AG, Kothawala DN, Attermeyer K, Tessier E, Bodmer P, Ledesma JLJ, Audet J, Casas-Ruiz JP, Catalán N, Cauvy-Fraunié S, Colls M, Deininger A, Evtimova VV, Fonvielle JA, Fuß T, Gilbert P, Herrero Ortega S, Liu L, Mendoza-Lera C, Monteiro J, Mor JR, Nagler M, Niedrist GH, Nydahl AC, Pastor A, Pegg J, Gutmann Roberts C, Pilotto F, Portela AP, González-Quijano CR, Romero F, Rulík M, Amouroux D (2018) The interplay between total mercury, methylmercury and dissolved organic matter in fluvial systems: a latitudinal study across Europe. Water Res 144:172–182. https://doi.org/10.1016/j.watres.2018.06.064
Dórea JG, Farina M, Rocha JBT (2013) Toxicity of ethylmercury (and Thimerosal): a comparison with methylmercury. J Appl Toxicol 33:700–711. https://doi.org/10.1002/jat.2855
Molina CI, Gibon F-M, Sánchez Y, et al (2010) Implicancia ambiental del mercurio en ecosistemas acuáticos de la Amazonía: Situación en Bolivia. Rev Virtual REDESMA Oct 4
Cristina M, Jardim WF (2004) O COMPORTAMENTO DO METILMERCÚRIO (METILHg) NO AMBIENTE Márcia. Quim Nova 27:593–600
Crespo-López ME, Macêdo GL, Pereira SID et al (2009) Mercury and human genotoxicity: critical considerations and possible molecular mechanisms. Pharmacol Res 60:212–220. https://doi.org/10.1016/j.phrs.2009.02.011
Woods JS, Heyer NJ, Russo JE, Martin MD, Farin FM (2014) Genetic polymorphisms affecting susceptibility to mercury neurotoxicity in children: summary findings from the casa Pia Children’s amalgam clinical trial. Neurotoxicology 44:288–302. https://doi.org/10.1016/j.neuro.2014.07.010
Arrifano GPF, de Oliveira MA, Souza-Monteiro JR, Paraense RO, Ribeiro-Dos-Santos A, Vieira JRDS, Silva ALDC, Macchi BM, do Nascimento JLM, Burbano RMRC-LM (2018) Role for apolipoprotein E in neurodegeneration and mercury intoxication. Front Biosci 1:229–241. https://doi.org/10.2741/e819
Sakamoto M, Tatsuta N, Izumo K et al (2018) Health impacts and biomarkers of prenatal exposure to Methylmercury: lessons from Minamata, Japan. Toxics 6:45. https://doi.org/10.3390/toxics6030045
Sakaue M, Mori N, Makita M, Fujishima K, Hara S, Arishima K, Yamamoto M (2009) Acceleration of methylmercury-induced cell death of rat cerebellar neurons by brain-derived neurotrophic factor in vitro. Brain Res 1273:155–162. https://doi.org/10.1016/j.brainres.2009.03.035
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
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 Health Part B 19:380–409. https://doi.org/10.1080/10937404.2016.1215772
Branco V, Caito S, Farina M, Teixeira da Rocha J, Aschner M, Carvalho C (2017) Biomarkers of mercury toxicity: past, present, and future trends. J Toxicol Environ Health B Crit Rev 20:119–154. https://doi.org/10.1080/10937404.2017.1289834
Yancheva V, Velcheva I, Stoyanova S, Georgieva (2016) Histological biomarkers in fish as a tool in ecological risk assessment and monitoring programs: a review. https://doi.org/10.15666/aeer/1401_047075
Bittarello AC, Vieira JCS, Braga CP, de Paula Araújo WL, da Cunha Bataglioli I, da Silva JM, Buzalaf MAR, Fleuri LF, de Magalhães Padilha P (2019) Characterization of molecular biomarkers of mercury exposure to muscle tissue of Plagioscion squamosissimus and Colossoma macropomum from the Amazon region. Food Chem 276:247–254. https://doi.org/10.1016/j.foodchem.2018.10.002
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
Vieira JCS, Braga CP, de Oliveira G et al (2018) Correction to: mercury exposure: protein biomarkers of mercury exposure in Jaraqui fish from the Amazon region. Biol Trace Elem Res 183:172–172. https://doi.org/10.1007/s12011-017-1195-8
Vieira JCS, Braga CP, de Oliveira G et al (2017) Identification of protein biomarkers of mercury toxicity in fish. Environ Chem Lett 15:717–724. https://doi.org/10.1007/s10311-017-0644-0
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
UniProt (2016) Universal Protein Resource (UniProt). In: 2016
Cerbino MR, Vieira JCS, Braga CP, Oliveira G, Padilha IF, Silva TM, Zara LF, Silva NJ Jr, Padilha PM (2017) Metalloproteomics approach to analyze mercury in breast Milk and hair samples of lactating women in communities of the Amazon Basin, Brazil. Biol Trace Elem Res 181:1–11. https://doi.org/10.1007/s12011-017-1057-4
de Castro NSS, Lima MDO (2014, 2014) Biomarkers of mercury exposure in the Amazon. Biomed Res Int. https://doi.org/10.1155/2014/867069
Gutiérrez-Mosquera H, Sujitha SB, Jonathan MP et al (2018) Mercury levels in human population from a mining district in Western Colombia. J Environ Sci 68:83–90. https://doi.org/10.1016/j.jes.2017.12.007
Wolf SE, Swaddle JP, Cristol DA, Buchser WJ (2017) Methylmercury exposure reduces the auditory brainstem response of Zebra finches (Taeniopygia guttata ). J Assoc Res Otolaryngol 18:569–579. https://doi.org/10.1007/s10162-017-0619-7
Zhou F, Yin G, Gao Y et al (2019) Toxicity assessment due to prenatal and lactational exposure to lead, cadmium and mercury mixtures. Environ Int 133. https://doi.org/10.1016/j.envint.2019.105192
de Queiroz JV, Vieira JCS, da Cunha BI et al (2018) Total mercury determination in muscle and liver tissue samples from Brazilian Amazon fish using slurry sampling. Biol Trace Elem Res 184:517–522. https://doi.org/10.1007/s12011-017-1212-y
Sénèque O, Rousselot-Pailley P, Pujol A, Boturyn D, Crouzy S, Proux O, Manceau A, Lebrun C, Delangle P (2018) Mercury trithiolate binding (HgS 3 ) to a de novo designed cyclic decapeptide with three preoriented cysteine side chains. Inorg Chem 57:2705–2713. https://doi.org/10.1021/acs.inorgchem.7b03103
Fiati Kenston SS, Su H, Li Z, Kong L, Wang Y, Song X, Gu Y, Barber T, Aldinger J, Hua Q, Li Z, Ding M, Zhao J, Lin X (2018) The systemic toxicity of heavy metal mixtures in rats. Toxicol Res (Camb) 7:396–407. https://doi.org/10.1039/c7tx00260b
Vieira JCS, Braga CP, de Oliveira G et al (2017) Correction to: mercury exposure: protein biomarkers of mercury exposure in Jaraqui fish from the Amazon region. Biol Trace Elem Res 1. https://doi.org/10.1007/s12011-017-1195-8
De Queiroz JV, Cavalcante J, Vieira S et al (2018) Identification of biomarkers of mercury contamination in Brachyplatystoma filamentosum of the Madeira River. Using Metalloproteomic Strategies, Brazil
Kumeta H, Nakayama H, Ogura K (2017) Solution structure of the major fish allergen parvalbumin Sco j 1 derived from the Pacific mackerel. Sci Rep 7:17160. https://doi.org/10.1038/s41598-017-17281-6
Freidl R, Gstöttner A, Baranyi U, et al (2019) Resistance of parvalbumin to gastrointestinal digestion is required for profound and long-lasting prophylactic oral tolerance. Allergy all.13994. https://doi.org/10.1111/all.13994
Vologzhannikova AA, Khorn PA, Kazakov AS, Ismailov RG, Sokolov AS, Uversky VN, Permyakov EA, Permyakov SE (2017) In search for globally disordered apo-parvalbumins: case of parvalbumin β-1 from coho salmon. Cell Calcium 67:53–64. https://doi.org/10.1016/j.ceca.2017.08.011
Dudev T, Lim C (2014) Competition among metal ions for protein binding sites: determinants of metal ion selectivity in proteins. Chem Rev 114:538–556. https://doi.org/10.1021/cr4004665
Kumar VD, Lee L, Edwards BFP (1991) Refined crystal structure of ytterbium-substituted carp parvalbumin 4.25 at 1.5 Å, and its comparison with the native and cadmium-substituted structures. FEBS Lett 283:311–316. https://doi.org/10.1016/0014-5793(91)80616-B
Svärd M, Drakenberg T (1986) Cation binding to parvalbumin studied by 113Cd and 23Na NMR. Peak assignment of rabbit (pI 5.5) parvalbumin. Acta Chem Scand B 40:689–693. https://doi.org/10.3891/acta.chem.scand.40b-0689
(2018) rps27a - precursor da proteína S27a ribossômica ubiquitina-40S - Ictalurus punctatus (catfish canal) - gene rps27a & proteína
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. https://doi.org/10.1007/s12011-012-9502-x
Han M-HJ, Hu Z, Chen CY et al (2014) Dysbindin-associated proteome in the p2 synaptosome fraction of mouse brain. J Proteome Res 13:4567–4580. https://doi.org/10.1021/pr500656z
Falini G, Fermani S, Tosi G, Arnesano F, Natile G (2008) Structural probing of Zn(II), cd(II) and hg(II) binding to human ubiquitin. Chem Commun:5960–5962. https://doi.org/10.1039/b813463d
Furuchi T, Hwang GW, Naganuma A (2002) Overexpression of the ubiquitin-conjugating enzyme Cdc34 confers resistance to methylmercury in Saccharomyces cerevisiae. Mol Pharmacol 61:738–741. https://doi.org/10.1124/mol.61.4.738
Kurita H, Hasegawa T, Seko Y, Nagase H, Tokumoto M, Lee JY, Satoh M (2018) Effect of gestational cadmium exposure on fetal growth, polyubiquitinated protein and monoubiqutin levels in the fetal liver of mice. J Toxicol Sci 43:19–24
Ugone V, Sanna D, Sciortino G, Maréchal JD, Garribba E (2019) Interaction of vanadium(IV) species with ubiquitin: a combined instrumental and computational approach. Inorg Chem 58:8064–8078. https://doi.org/10.1021/acs.inorgchem.9b00807
Funding
The authors thank the Brazilian Research Funding Agencies (FAPESP) (processes 2013/21297-1 and 2014/02668-1), the Coordination of Improvement of Higher Level Personnel (Capes), and the National Electric Energy Agency (ANEEL).
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All the work involved with animal experimentation developed in this paper was approved by the Ethics Committee on the Use of Animals (CEUA) of the Faculty of Veterinary Medicine and Zootechnics (FMVZ) of the São Paulo State University (UNESP), School of Veterinary Medicine and Animal Science, Botucatu, Brazil under the number of protocol 110/2015.
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Vieira, J.C.S., de Oliveira, G., Braga, C.P. et al. Parvalbumin and Ubiquitin as Potential Biomarkers of Mercury Contamination of Amazonian Brazilian Fish. Biol Trace Elem Res 197, 667–675 (2020). https://doi.org/10.1007/s12011-020-02026-w
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DOI: https://doi.org/10.1007/s12011-020-02026-w