Abstract
The mangrove crab Ucides cordatus is a bioindicator of aquatic contamination. In this work, the iron availability and redox activity of saccharide-coated mineral iron supplements (for both human and veterinary use) and ferrocene derivatives in Saline Ucides Buffer (SUB) medium were assessed. The transport of these metallodrugs by four different hepatopancreatic cell types (embryonic (E), resorptive (R), fibrillar (F), and blister (B)) of U. cordatus were measured. Organic coated iron minerals (iron supplements) were stable against strong chelators (calcein and transferrin). Ascorbic acid efficiently mediated the release of iron only from ferrocene compounds, leading to redox-active species. Ferrous iron and iron supplements were efficient in loading iron to all hepatopancreatic cell types. In contrast, ferrocene derivatives were loaded only in F and B cell types. Acute exposition to the iron compounds resulted in cell viability of 70–95%, and to intracellular iron levels as high as 0.40 μmol L−1 depending upon the compound and the cell line. The easiness that iron from iron metallodrugs was loaded/transported into U. cordatus hepatopancreatic cells reinforces a cautionary approach to the widespread disposal and use of highly bioavailable iron species as far as the long-term environmental welfare is concerned.
Similar content being viewed by others
References
Ahearn GA, Duerr JM, Zhuang Z, Brown RJ, Aslamkhan A, Killebrew DA (1999) Ion transport processes of crustacean epithelial cells. Physiol Biochem Zool 72:1–18. https://doi.org/10.1086/316643
Ahearn GA, Mandal PK, Mandal A (2004) Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review. J Comp Physiol B 174:439–452. https://doi.org/10.1007/s00360-004-0438-0
Andrews NC (2000) Iron homeostasis: insights from genetics and animal models. Nat Rev Genet 1:208–217. https://doi.org/10.1038/35042073
Bound JP, Kitsou K, Voulvoulis N (2006) Household disposal of pharmaceuticals and perception of risk to the environment. Environ Toxicol Pharmacol 21:301–307. https://doi.org/10.1016/j.etap.2005.09.006
Breuer W, Cabantchik ZI (2001) A fluorescence-based one-step assay for serum non-transferrin-bound iron. Anal Biochem 299:194–202. https://doi.org/10.1006/abio.2001.5378
Breuer W, Epsztejn S, Cabantchik ZI (1995) Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron(II). J Biol Chem 270:24209–24215. https://doi.org/10.1074/jbc.270.41.24209
Cairo G, Bernuzzi F, Recalcati S (2006) A precious metal: iron, an essential nutrient for all cells. Genes Nutr 1:25–39. https://doi.org/10.1007/BF02829934
Chavez-Crooker P, Garrido N, Ahearn GA (2001) Copper transport by lobster hepatopancreatic epithelial cells separated by centrifugal elutriation: measurements with the fluorescent dye Phen Green. J Exp Biol 204:1433–1444
Chavez-Crooker P, Garrido N, Pozo P, Ahearn GA (2003a) Copper transport by lobster (Homarus americanus) hepatopancreatic lysosomes. Comp Biochem Physiol C Toxicol Pharmacol 135:107–118
Chavez-Crooker P, Pozo P, Castro H, Dice MS, Boutet I, Tanguy A, Moraga D, Ahearn GA (2003b) Cellular localization of calcium, heavy metals, and metallothionein in lobster (Homarus americanus) hepatopancreas. Comp Biochem Physiol C Toxicol Pharmacol 136:213–224
Corrêa Junior JD, Allodi S, Amado-Filho GM, Farina M (2000) Zinc accumulation in phosphate granules of Ucides cordatus hepatopancreas. Braz J Med Biol Res 33:217–221. https://doi.org/10.1590/S0100-879X2000000200009
Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902. https://doi.org/10.1146/annurev.biochem.78.081307.110540
Donadel K, Felisberto MDV, Fávere VT, Rigoni M, Batistela NJ, Laranjeira MCM (2008) Synthesis and characterization of the iron oxide magnetic particles coated with chitosan biopolymer. Mater Sci Eng C 28:509–514. https://doi.org/10.1016/J.MSEC.2007.06.004
Esposito BP (2003) Labile plasma iron in iron overload: redox activity and susceptibility to chelation. Blood 102:2670–2677. https://doi.org/10.1182/blood-2003-03-0807
Espósito BP, Epsztejn S, Breuer W, Cabantchik ZI (2002) A review of fluorescence methods for assessing labile iron in cells and biological fluids. Anal Biochem 304:1–18. https://doi.org/10.1006/abio.2002.5611
Esposito BP, Breuer W, Sirankapracha P, Pootrakul P, Hershko C, Cabantchik ZI (2003) Labile plasma iron in iron overload: redox activity and susceptibility to chelation. Blood 102:2670–2677. https://doi.org/10.1182/blood-2003-03-0807
Gagné F (2014) Chapter 6: oxidative stress. In: Biochemical ecotoxicology. Academic press, Oxford, pp 103–115
Gil E d S et al (2007) Aspectos técnicos e legais do gerenciamento de resíduos químico-farmacêuticos. Rev Bras Ciências Farm 43:19–29. https://doi.org/10.1590/S1516-93322007000100003
Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1–14
Hirsch GC, Buchmann W (1930) Der Arbeitsrhythmus der Mitteldarmdruse von Astacus leptodactylus. Z Vgl Physiol 12:559–578. https://doi.org/10.1007/BF00337897
Kasprzyk-Hordern B, Dinsdale RM, Guwy AJ (2009) The removal of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs during wastewater treatment and its impact on the quality of receiving waters. Water Res 43:363–380. https://doi.org/10.1016/j.watres.2008.10.047
Huebers HA, Huebers E, Finch CA, Martin AW (1982) Characterization of an invertebrate transferrin from the crab Cancer magister (Arthropoda)
Kang X, Mu S, Li W, Zhao N (2012) Toxic effects of cadmium on crabs and shrimps. In: Toxicity and drug testing. InTech,
Liu Z-Q (2011) Potential applications of ferrocene as a structural feature in antioxidants. Mini Rev Med Chem 11:345–358
Marcolin CR, Carqueija CRG, de Tozetto SO et al (2008) Alterações morfológicas do hepatopâncreas de Ucides cordatus (Linnaeus, 1763) (Crustacea, Decapoda, Ocypodidae) em relação aos estádios de intermuda e pré-muda inicial. Rev Bras Zoociências 10:97–104
Meneghini R (1997) Iron homeostasis, oxidative stress, and DNA damage. Free Radic Biol Med 23:783–792. https://doi.org/10.1016/S0891-5849(97)00016-6
Muench KH (1989) Hemochromatosis and infection: alcohol and iron, oysters and sepsis. Am J Med 87:40N–43N
Naidu KA (2003) Vitamin C in human health and disease is still a mystery? An overview. Nutr J 2:7. https://doi.org/10.1186/1475-2891-2-7
Nielsen P, Heinrich HC (1993) Metabolism of iron from (3,5,5-trimethylhexanoyl) ferrocene in rats. Biochem Pharmacol 45:385–391. https://doi.org/10.1016/0006-2952(93)90074-7
Ortega P, e Sá MG, Custódio MR, Zanotto FP (2011) Separation and viability of gill and hepatopancreatic cells of a mangrove crab Ucides cordatus. Vitr Cell Dev Biol-Anim 47:346–349. https://doi.org/10.1007/s11626-011-9402-y
Ortega P, Custódio MR, Zanotto FP (2014a) Characterization of cadmium plasma membrane transport in gills of a mangrove crab Ucides cordatus. Aquat Toxicol 157:21–29. https://doi.org/10.1016/j.aquatox.2014.09.006
Ortega P, Santos RA, Lacouth P, Rozas EE, Custódio MR, Zanotto FP (2014b) Cytochemical characterization of gill and hepatopancreatic cells of the crab Ucides cordatus (Crustacea, Brachyura) validated by cell metal transport. Iheringia Série Zool 104:347–354. https://doi.org/10.1590/1678-476620141043347354
Ortega P, Vitorino HA, Moreira RG, Pinheiro MAA, Almeida AA, Custódio MR, Zanotto FP (2016) Physiological differences in the crab Ucides cordatus from two populations inhabiting mangroves with different levels of cadmium contamination. Environ Toxicol Chem 9999:1–11. https://doi.org/10.1002/etc.3537
Pinheiro MAA, Duarte LFA, Toledo TR, Adam ML, Torres RA (2013) Habitat monitoring and genotoxicity in Ucides cordatus (Crustacea: Ucididae), as tools to manage a mangrove reserve in southeastern Brazil. Environ Monit Assess 185:8273–8285. https://doi.org/10.1007/s10661-013-3172-9
Pinto JP, Arezes J, Dias V, Oliveira S, Vieira I, Costa M, Vos M, Carlsson A, Rikers Y, Rangel M, Porto G (2014) Physiological implications of NTBI uptake by T lymphocytes. Front Pharmacol 5:24. https://doi.org/10.3389/fphar.2014.00024
Praschberger M, Haider K, Cornelius C, Schitegg M, Sturm B, Goldenberg H, Scheiber-Mojdehkar B (2015) Iron sucrose and ferric carboxymaltose: no correlation between physicochemical stability and biological activity. Biometals 28:35–50. https://doi.org/10.1007/s10534-014-9801-0
Sá MG, Zanotto FP (2013) Characterization of copper transport in gill cells of a mangrove crab Ucides cordatus. Aquat Toxicol 144–145:275–283. https://doi.org/10.1016/j.aquatox.2013.10.018
Saravanan M, Suganya R, Ramesh M, Poopal RK, Gopalan N, Ponpandian N (2015) Iron oxide nanoparticles induced alterations in haematological, biochemical and ionoregulatory responses of an Indian major carp Labeo rohita. J Nanopart Res 17:274. https://doi.org/10.1007/s11051-015-3082-6
Topham R, Cooper B, Tesh S, Godette G, Bonaventura C, Bonaventura J (1988) Isolation, purification and characterization of an iron-binding protein from the horseshoe crab (Limulus polyphemus). Biochem J 252:151–157
Viarengo A, Nott JA (1993) Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp Biochem Physiol Part C Comp Pharmacol 104:355–372. https://doi.org/10.1016/0742-8413(93)90001-2
Vitorino HA, Mantovanelli L, Zanotto FP, Espósito BP (2015) Iron metallodrugs: stability, redox activity and toxicity against Artemia salina. PLoS One 10:e0121997. https://doi.org/10.1371/journal.pone.0121997
Conflict of interest
The authors declare that they have no conflicts of interest.
Funding
The authors acknowledge the funding provided through the CAPES and FAPESP (Brazilian government agencies). H.A.V. and P.O. received a Doctoral Fellowship from CAPES.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Cinta Porte
Rights and permissions
About this article
Cite this article
Vitorino, H.A., Ortega, P., Pastrana Alta, R.Y. et al. Evaluation of iron loading in four types of hepatopancreatic cells of the mangrove crab Ucides cordatus using ferrocene derivatives and iron supplements. Environ Sci Pollut Res 25, 15962–15970 (2018). https://doi.org/10.1007/s11356-018-1819-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-1819-3