Skip to main content
SpringerLink
Log in

Identification of Zinc Absorption Biomarkers in Muscle Tissue of Nile Tilapia Fed with Organic and Inorganic Sources of Zinc Using Metallomics Analysis

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

The development of metallomics techniques has allowed for metallomics analysis of biological systems, enabling a better understanding of the response mechanisms for different stimuli, their relationship to metallic species, and the characterization of biomarkers. In this study, a metallomics analysis of the muscle tissue of Nile tilapia was used to aid the understanding of the molecular mechanisms involved in zinc absorption in this fish species when fed organic and/or inorganic sources of zinc and to identify possible biomarkers for the absorption of this micromineral. To accomplish this, the fish were separated into three groups of 24 g, 74 g, and 85 g initial weights, and each group, respectively, was fed a zinc-free diet (control group, G1), a diet containing zinc found in organic sources (treatment 1, G2), and a diet containing zinc from an inorganic source (treatment 2, G3). Two-dimensional polyacrylamide (2D PAGE) gel electrophoresis was used to separate the proteins of the muscle tissue. Subsequently, the expression profiles of protein spots in the samples where zinc was applied in different concentrations were compared, using the software ImageMaster 2D Platinum version 7.0, to identify proteins that were differentially expressed. The identified proteins were then exposed to atomic absorption spectrometry in a graphite furnace to determine zinc mapping and were subsequently characterized via electrospray ionization tandem mass spectrometry (ESI-MS/MS). The metallomic analysis identified 15 proteins differentially expressed and associated with zinc, leading to the conclusion that three metal-binding proteins presented as possible biomarkers of zinc absorption in fish.

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
Fig. 3

Similar content being viewed by others

References

  1. Garcia JS, de MCS, Arruda MAZ (2006) Trends in metal-binding and metalloprotein analysis. Talanta 69:1–15. https://doi.org/10.1016/j.talanta.2005.08.041

    Article  CAS  PubMed  Google Scholar 

  2. Szpunar J (2004) Metallomics: a new frontier in analytical chemistry. Anal Bioanal Chem 378:54–56. https://doi.org/10.1007/s00216-003-2333-z

    Article  CAS  PubMed  Google Scholar 

  3. Haraguchi H (2004) Metallomics as integrated biometal science. J Anal At Spectrom 19:5. https://doi.org/10.1039/b308213j

    Article  CAS  Google Scholar 

  4. Council NR (2011) Nutrient requirements of fish and shrimp. https://doi.org/10.17226/13039

    Book  Google Scholar 

  5. Miller J, Ramsey NMF (1993) Efecto de la raza sobre la acumulación de cobre en terneros de cebo - Google Livros, vol 1993, pp 391–457

    Google Scholar 

  6. McDowell LR (2001) Recent advanced in minerals and vitamins on nutrition of lactating cows. In: Simpósio Internacional em Bovinocultura de Leite, pp 51–76

    Google Scholar 

  7. Apines MJ, Satoh S, Kiron V, Watanabe T, Nasu N, Fujita S (2001) Bioavailability of amino acids chelated and glass embedded zinc to rainbow trout, Oncorhynchus mykiss, fingerlings. Aquac Nutr 7:221–228. https://doi.org/10.1046/j.1365-2095.2001.00178.x

    Article  CAS  Google Scholar 

  8. Vallee BL, Falchuk KH (1993) The biochemical basis of zinc physiology. Physiol Rev 73:79–118. https://doi.org/10.1152/physrev.1993.73.1.79

    Article  CAS  PubMed  Google Scholar 

  9. Maret W (2010) Metalloproteomics, metalloproteomes, and the annotation of metalloproteins. Metallomics 2:117–125. https://doi.org/10.1039/B915804A

    Article  CAS  PubMed  Google Scholar 

  10. Maret W, Vallee BL (1998) Thiolate ligands in metallothionein confer redox activity on zinc clusters. Proc Natl Acad Sci U S A 95:3478–3482

    Article  CAS  Google Scholar 

  11. Khaled S, Brun JF, Bardet L, Cassanas G (1997) Importance physiologique du zinc dans l’activité physique. Sci Sports 12:179–191. https://doi.org/10.1016/S0765-1597(97)84576-5

    Article  Google Scholar 

  12. Bachere E, Gueguen Y, Gonzalez M, de Lorgeril J, Garnier J, Romestand B (2004) Insights into the anti-microbial defense of marine invertebrates: the penaeid shrimps and the oyster Crassostrea gigas. Immunol Rev 198:149–168. https://doi.org/10.1111/j.0105-2896.2004.00115.x

    Article  CAS  PubMed  Google Scholar 

  13. Cerenius L (1994) The journal of biological chemistry. American Society for Biochemistry and Molecular Biology, Rockville

    Google Scholar 

  14. Lima PM, Neves R de CF, 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

    Article  CAS  PubMed  Google Scholar 

  15. Braga CP, Bittarello AC, Padilha CCF, Leite AL, Moraes PM, Buzalaf MAR, Zara LF, Padilha PM (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

    Article  CAS  PubMed  Google Scholar 

  16. Sampaio Gonçalves G, Edivaldo Pezzato L, Maria Barros M et al (2009) Energia E Nutrientes Digestíveis De Alimentos Para a Tilápia Do Nilo* Digestible Nutrients of Nile Tilapia Feed. B Inst Pesca, São Paulo 35:201–213

    Google Scholar 

  17. Guimarães IG, Pezzato LE, Barros MM (2008) Amino acid availability and protein digestibility of several protein sources for Nile tilapia, Oreochromis niloticus. Aquac Nutr 14:396–404. https://doi.org/10.1111/j.1365-2095.2007.00540.x

    Article  CAS  Google Scholar 

  18. Edivaldo Pezzato L, Carvalho de Miranda E, Maria Barros M, et al (2002) Digestibilidade Aparente de Ingredientes pela Tilápia do Nilo (Oreochromis niloticus) apparent digestibility of feedstuffs by Nile Tilapia (Oreochromis niloticus)

    Google Scholar 

  19. Vieira JCS, de Queiroz JV, do Carmo Federici Padilha C et al (2017) 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

    Article  CAS  PubMed  Google Scholar 

  20. Doumas BT, Bayse DD, Borner K et al (1981) A candidate reference method for determination of total protein in serum II. Test for Transferability. Clin Chem 271027:1651–1654

    Article  Google Scholar 

  21. Pereira Braga C, Cavalcante Souza Vieira J, de LLA et al (2017) Metalloproteomic and differential expression in plasma in a rat model of type 1 diabetes. Int J Biol Macromol 104:414–422. https://doi.org/10.1016/j.ijbiomac.2017.06.032

    Article  CAS  PubMed  Google Scholar 

  22. Lima PM, Cavecci B, Roldan P dos S et al (2016) Zinc determination in samples fish by GFAAS using acid digestion in an ultrasound bath. J Food Meas Charact 10:113–118. https://doi.org/10.1007/s11694-015-9283-y

    Article  Google Scholar 

  23. de Lima PM, Cavecci B, Roldan P dos S et al (2016) Zinc determination in samples fish by GFAAS using acid digestion in an ultrasound bath. J Food Meas Charact 10:113–118. https://doi.org/10.1007/s11694-015-9283-y

    Article  Google Scholar 

  24. Currie LA (1999) Nomenclature in evaluation of analytical methods including detection and quantification capabilities1Adapted from the International Union of Pure and Applied Chemistry (IUPAC) document nomenclature in evaluation of analytical methods including detection. Anal Chim Acta 391:105–126. https://doi.org/10.1016/S0003-2670(99)00104-X

    Article  CAS  Google Scholar 

  25. Shevchenko A, Tomas H, Havliš J et al (2007) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856–2860. https://doi.org/10.1038/nprot.2006.468

    Article  CAS  Google Scholar 

  26. Braga CP, Vieira JCS, Grove RA, Boone CHT, Leite AL, Buzalaf MAR, Fernandes AAH, Adamec J, Padilha PM (2017) A proteomic approach to identify metalloproteins and metal-binding proteins in liver from diabetic rats. Int J Biol Macromol 96:817–832. https://doi.org/10.1016/j.ijbiomac.2016.12.073

    Article  CAS  PubMed  Google Scholar 

  27. Li GZ, Vissers JPC, Silva JC, Golick D, Gorenstein MV, Geromanos SJ (2009) Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures. Proteomics 9:1696–1719. https://doi.org/10.1002/pmic.200800564

    Article  CAS  PubMed  Google Scholar 

  28. Berbel P, Marco P, Cerezo J, DeFelipe J (1996) Distribution of parvalbumin immunoreactivity in the neocortex of hypothyroid adult rats. Neurosci Lett 204:65–68. https://doi.org/10.1016/0304-3940(96)12318-1

    Article  CAS  PubMed  Google Scholar 

  29. Coughlin DJ, Solomon S, Wilwert JL (2007) Parvalbumin expression in trout swimming muscle correlates with relaxation rate. Comp Biochem Physiol A Mol Integr Physiol 147:1074–1082. https://doi.org/10.1016/j.cbpa.2007.03.020

    Article  CAS  PubMed  Google Scholar 

  30. Tusnády GE, Simon I (1998) Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol 283:489–506. https://doi.org/10.1006/jmbi.1998.2107

    Article  PubMed  Google Scholar 

  31. Conrad M, Lemb K, Schubert T, Markl J (1998) Biochemical identification and tissue-specific expression patterns of keratins in the zebrafish Danio rerio. Cell Tissue Res 293:195–205

    Article  CAS  Google Scholar 

  32. Snider NT (2016) Kidney keratins: cytoskeletal stress responders with biomarker potential. Kidney Int 89:738–740. https://doi.org/10.1016/J.KINT.2015.12.040

    Article  CAS  PubMed  Google Scholar 

  33. Bose A, Teh M-T, Mackenzie I, Waseem A (2013) Keratin K15 as a biomarker of epidermal stem cells. Int J Mol Sci 14:19385–19398. https://doi.org/10.3390/ijms141019385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lerner MB, Kybert N, Mendoza R, Villechenon R, Bonilla Lopez MA, Charlie Johnson AT (2013) Scalable, non-invasive glucose sensor based on boronic acid functionalized carbon nanotube transistors. Appl Phys Lett 102:183113. https://doi.org/10.1063/1.4804438

    Article  CAS  Google Scholar 

  35. Cortes M, Wong E, Koipally J, Georgopoulos K (1999) Control of lymphocyte development by the Ikaros gene family. Curr Opin Immunol 11:167–171. https://doi.org/10.1016/S0952-7915(99)80028-4

    Article  CAS  PubMed  Google Scholar 

  36. Melov S, Vaughan H, Cotterill S, Cotterill S (1992) Molecular characterisation of the gene for the 180 kDa subunit of the DNA polymerase-primase of Drosophila melanogaster. J Cell Sci 102(Pt 4):847–856

    CAS  PubMed  Google Scholar 

  37. Ohtsuka K, Hata M (2000) Molecular chaperone function of mammalian Hsp70 and Hsp40 - a review. Int J Hyperth 16:231–245. https://doi.org/10.1080/026567300285259

    Article  CAS  Google Scholar 

  38. Wang Y, Xu J, Sheng L, Zheng Y (2007) Field and laboratory investigations of the thermal influence on tissue-specific Hsp70 levels in common carp (Cyprinus carpio). Comp Biochem Physiol A Mol Integr Physiol 148:821–827. https://doi.org/10.1016/J.CBPA.2007.08.009

    Article  PubMed  Google Scholar 

  39. Efremova SM, Margulis BA, Guzhova IV, Itskovich VB, Lauenroth S, Müller WEG, Schröder HC (2002) Heat shock protein Hsp70 expression and DNA damage in Baikalian sponges exposed to model pollutants and wastewater from Baikalsk pulp and paper plant. Aquat Toxicol 57:267–280. https://doi.org/10.1016/S0166-445X(01)00209-0

    Article  CAS  PubMed  Google Scholar 

  40. Tomanek L (2008) The importance of physiological limits in determining biogeographical range shifts due to global climate change: the heat-shock response. Physiol Biochem Zool: PBZ 81:709–717. https://doi.org/10.1086/590163

    Article  CAS  PubMed  Google Scholar 

  41. Jonsson H, Schiedek D, Goksøyr A, Grøsvik BE (2006) Expression of cytoskeletal proteins, cross-reacting with anti-CYP1A, in Mytilus sp. exposed to organic contaminants. Aquat Toxicol 78:S42–S48. https://doi.org/10.1016/j.aquatox.2006.02.014

    Article  CAS  PubMed  Google Scholar 

  42. Chevalier C, Le Querrec F, Raymond P (1996) Sugar levels regulate the expression of ribosomal protein genes encoding protein S28 and ubiquitin-fused protein S27a in maize primary root tips. Plant Sci 117:95–105. https://doi.org/10.1016/0168-9452(96)04399-3

    Article  CAS  Google Scholar 

  43. Silva TA da (2015) Aspectos reprodutivos e produtivos de carneiros de raça morada nova submetidos a níveis crescentes de suplementaçaõ concentrada. Repositorio.ufc.br 1:1–74

  44. Clayton DA (2000) Transcription and replication of mitochondrial DNA. Hum Reprod 15:11–17. https://doi.org/10.1093/humrep/15.suppl_2.11

    Article  PubMed  Google Scholar 

  45. 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

    Article  CAS  Google Scholar 

  46. Cavecci B, de LPM, de QJV et al (2014) Metalloproteomic profile determination of muscle samples from Nile Tilapia ( Oreochromis niloticus ) using AAS and ESI-MS/MS after 2D-PAGE separation. J Braz Chem Soc 26:239–246. https://doi.org/10.5935/0103-5053.20140260

    Article  CAS  Google Scholar 

  47. Berenbrink M, Koldkjaer P, Kepp O et al (2005) Evolution of oxygen secretion in fishes and the emergence of a complex physiological system. Science (New York, NY) 307:1752–1757. https://doi.org/10.1126/science.1107793

    Article  CAS  Google Scholar 

  48. Challis GL, Ravel J, Townsend CA (2000) Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem Biol 7:211–224. https://doi.org/10.1016/S1074-5521(00)00091-0

    Article  CAS  PubMed  Google Scholar 

  49. Shi Y (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139:468–484. https://doi.org/10.1016/J.CELL.2009.10.006

    Article  CAS  PubMed  Google Scholar 

  50. Bhavsar RB, Makley LN, Tsonis PA (2010) The other lives of ribosomal proteins. Hum Genomics 4:327–344. https://doi.org/10.1186/1479-7364-4-5-327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Moorthamer M, Chaudhuri B (1999) Identification of ribosomal protein L34 as a novel Cdk5 inhibitor. Biochem Biophys Res Commun 255:631–638. https://doi.org/10.1006/bbrc.1999.0145

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the Foundation for Research Support of the São Paulo State — FAPESP (process 2010/51562-0 and 2010/51332-5) and the National Council of Scientific and Technological Development — CNPq (process 472388/2011-8).

Author information

Authors and Affiliations

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

    Paula Monteiro de Lima, Bruna Cavecci-Mendonça, Luiz Edivaldo Pezzato & Pedro de Magalhães Padilha

  2. Institute of Biosciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil

    José Cavalcante Souza Vieira, Luciana Francisco Fleuri & Pedro de Magalhães Padilha

  3. Federal University of Mato Grosso do Sul (UFMS), Campo Grande, Brazil

    José Cavalcante Souza Vieira

  4. Biochemistry Department, São Paulo University (USP), Bauru, São Paulo, Brazil

    Aline de Lima Leite & Marília Afonso Rabelo Buzalaf

  5. Biochemistry Department, University of Nebraska-UNL, Lincoln, NE, USA

    Camila Pereira Braga

Authors
  1. Paula Monteiro de Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Cavalcante Souza Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruna Cavecci-Mendonça
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luciana Francisco Fleuri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aline de Lima Leite
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marília Afonso Rabelo Buzalaf
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luiz Edivaldo Pezzato
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Camila Pereira Braga
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. 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.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 22988 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Lima, P.M., Vieira, J.C.S., Cavecci-Mendonça, B. et al. Identification of Zinc Absorption Biomarkers in Muscle Tissue of Nile Tilapia Fed with Organic and Inorganic Sources of Zinc Using Metallomics Analysis. Biol Trace Elem Res 194, 259–272 (2020). https://doi.org/10.1007/s12011-019-01765-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-019-01765-9

Keywords

Search

Navigation