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Original Articles

Copper uptake in adult rainbow trout irradiated during early life stages and in non-irradiated bystander trout which swam with the irradiated fish

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Pages 1130-1138 | Received 10 May 2020, Accepted 06 Sep 2021, Published online: 28 Sep 2021

References

  • Arif H, Sohail A, Farhan M, Abdur Rehman A, Ahmad A, Hadi SM. 2018. Flavonoids-induced redox cycling of copper ions leads to generation of reactive oxygen species: a potential role in cancer chemoprevention. Int J Biol Macromol. 106:569–578.
  • Blockhuys S, Wittung-Stafshede P. 2017. Copper chaperone Atox1 plays role in breast cancer cell migration. Biochem Biophys Res Commun. 483(1):301–304.
  • Brewer GJ. 2014. The promise of copper lowering therapy with tetrathiomolybdate in the cure of cancer and in the treatment of inflammatory disease. J Trace Elem Med Biol. 28(4):372–378.
  • Calderón-González KG, Rustarazo MLV, Labra-Barrios ML, Bazán-Méndez CI, Tavera-Tapia A, Herrera-Aguirre ME, Sánchez del Pino MM, Gellegos-Pérez JL, González-Márquez H, Hernández-Hernández JM, León-Ávila G, et al. 2015. Determination of the protein expression profiles of breast cancer cell lines by quantitative proteomics using ITRAQ labelling and tandem mass spectrometry. J Proteomics. 124:50–78.
  • Capo CR, Pedersen JZ, Falconi M, Rossi L. 2017. Oleuropein shows copper complexing properties and noxious effect on cultured SH-SY5Y neuroblastoma cells depending on cell copper content. J Trace Elem Med Biol. 44:225–232.
  • Chen W, Zou P, Zhao Z, Chen X, Fan X, Vinothkumar R, Cui R, Wu F, Zhang Q, Liang G, et al. 2016. Synergistic antitumor activity of rapamycin and EF24 via increasing ROS for the treatment of gastric cancer. Redox Biol. 10:78–89.
  • Chen X, Zhang X, Chen J, Yang Q, Yang L, Xu D, Zhang P, Wang X, Liu J. 2017. Hinokitiol copper complex inhibits proteasomal deubiquitination and induces paraptosis-like cell death in human cancer cells . Eur J Pharmacol. 815:147–155.
  • Chuthapisith S, Bean BE, Cowley G, Eremin JM, Samphao S, Layfield R, Kerr LD, Wiseman J, El-Sheemy M, Sreenivasan T, et al. 2009. Annexins in human breast cancer: possible predictors of pathological response to neoadjuvant chemotherapy. Eur J Cancer. 45(7):1274–1281.
  • Dakubo GD, Parr RL, Costello LC, Franklin RB, Thayer RE. 2006. Altered metabolism and mitochondrial genome in prostate cancer. J Clin Pathol. 59(1):10–16.
  • Đermadi D, Valo S, Pussila M, Reyhani N, Sarantaus L, Lalowski M, Baumann M, Nyström M. 2014. Inherited cancer predisposition sensitizes colonic mucosa to address western diet effects and putative cancer-predisposing changes on mouse proteome. J Nutr Biochem. 25(11):1196–1047.
  • Ebadi M, Swanson S. 1988. The status of zinc, copper and metallothionein in cancer patients. Prog Clin Biol Res. 259:161–175.
  • Farag AM, Boese CJ, Woodward DF, Bergman HL. 1994. Physiological changes and tissue metal accumulation in rainbow trout exposed to foodborne and waterborne metals. Environ Toxicol Chem. 13(12):2021–2029.
  • Feng X, Yu W, Zhou F, Chen J, Shen P. 2016. A novel small molecule compound diaporine inhibits breast cancer cell proliferation via promoting ROS generation. Biomed Pharmacother. 83:1038–1047.
  • Gellert M, Hanschmann E-M, Lepka K, Berndt C, Lillig CH. 2015. Redox regulation of cytoskeletal dynamics during differentiation and de-differentiation. Biochim Biophys Acta. 1850(8):1575–1587.
  • Gong E-Y, Shin YJ, Hwang L-Y, Kim JH, Kim S-M, Moon J-H, Shin J-S, Lee D-H, Hur DY, Jin D-H, et al. 2016. Combined treatment with vitamin C and sulindac synergistically induces p53- and ROS-dependent apoptosis in human colon cancer cells . Toxicol Lett. 258:126–133.
  • Grosell M, Wood CM. 2002. Copper uptake across rainbow trout gills: mechanisms of apical entry. J Exp Biol. 205(8):1179–1188.
  • Gupte A, Mumper RJ. 2009. Elevated copper and oxidative stress in cancer cells as a target for cancer treatment. Cancer Treat Rev. 35(1):32–46.
  • Hawas AH. 2013. The biosensitivity of certain organs in rats exposed to low doses of γ-radiation. J Rad Res Appl Sci. 6(2):56–62.
  • Hayes MJ, Moss SE. 2004. Annexins and disease. Biochem Biophys Acta. 1762:164–180.
  • He F, York JP, Burroughs SG, Qin L, Xia J, Chen D, Quigley EM, Webb P, LeSage GD, Xia X. 2015. Recruited metastasis suppressor NM23-H2 attenuates expression and activity of peroxisome proliferator-activated receptor δ (PPARδ) in human cholangiocarcinoma. Dig Liver Dis. 47(1):62–67.
  • Hillebrandt S, Streffer C. 1994. Protein patterns in tissues of foetuses with radiation-induced gastroschisis. Mutat Res. 308(1):11–22.
  • Koňarikova K, Perdikaris GA, Gbelcová H, Andrezálová L, Švéda M, Ruml T, Laubertová L, Režnáková S, Žitňanová I. 2016. Autophagy in MCF-7 cancer cells induced by copper complexes. Pharmacol Rep. 68(6):1221–1224.
  • Laurén DL, McDonald DG. 1987a. Acclimation to copper by rainbow trout, Salmo gairdneri: biochemistry. Can J Fish Aquat Sci. 44(1):105–111.
  • Laurén DL, McDonald DG. 1987b. Acclimation to copper by rainbow trout, Salmo gairdneri: physiology. Can J Fish Aquat Sci. 44(1):99–104.
  • Lee H-M, Patel V, Shyur L-F, Lee W-L. 2016. Copper supplementation amplifies the anti-tumor effect of curcumin in oral cancer cells. Phytomedicine. 23(12):1535–1544.
  • Linder MC. 2012. Review: The relationship of copper to DNA damage and damage prevention in humans. Mutat Res. 733(1-2):83–91.
  • Liu H, Zhang Y, Zheng S, Weng Z, Ma J, Li Y, Xie X, Zheng W. 2016. Detention of copper by sulfur nanoparticles inhibits the proliferation of A375 malignant melanoma and MCF-7 breast cancer cells. Biochem Biophys Res Commun. 477(4):1031–1037.
  • Lleonart ME. 2010. A new generation of proto-oncogenes: cold-inducible RNA binding proteins . Biochim Biophys Acta. 1805(1):43–52.
  • Lowndes SA, Harris AL. 2005. The role of copper in tumour angiogenesis. J Mammary Gland Biol Neoplasia. 10(4):299–310.
  • Mothersill C, Bucking C, Smith RW, Agnihotri N, Oneill A, Kilemade M, Seymour CB. 2006. Communication of radiation-induced stress or bystander signals between fish in vivo. Environ Sci Technol. 40(21):6859–6864.
  • Mothersill C, Rusin A, Fernandez-Palomo C, Seymour C. 2018. History of bystander effects research 1905-present; what is in a name? Int J Radiat Biol. 94(8):696–707.
  • Mothersill C, Seymour C. 2012. Changing paradigms in radiobiology. Mutat Res. 750(2):85–95.
  • Mothersill C, Smith RW, Agnihotri N, Seymour CB. 2007. Characterization of a radiation-induced stress response communicated in vivo between zebrafish. Environ Sci Technol. 41(9):3382–3387.
  • Mothersill C, Smith RW, Fazzari J, McNeill F, Prestwich W, Seymour CB. 2012. Evidence for a physical component to the radiation-induced bystander effect? Int J Radiat Biol. 88(8):583–591.
  • Mothersill C, Smith RW, Heier LS, Teien H-C, Lind OC, Land OC, Seymour CB, Oughton D, Salbu B. 2014. Radiation-induced bystander effects in the Atlantic salmon (salmo salar L.) following mixed exposure to copper and aluminum combined with low-dose gamma radiation. Radiat Environ Biophys. 53(1):103–114.
  • Mothersill C, Smith RW, Hinton TG, Aizawa K, Seymour CB. 2009. Communication of radiation-induced signals in vivo between DNA repair deficient and proficient medaka (Oryzias latipes). Environ Sci Technol. 43(9):3335–3342.
  • Mothersill C, Smith RW, Saroya R, Denbeigh J, Rowe B, Banevicius L, Timmins R, Moccia R, Seymour CB. 2010. Irradiation of rainbow trout at early life stages results in legacy effects in adults. Int J Radiat Biol. 86(10):817–828.
  • Mrdakovic Popic J, Salbu B, Skipperud L. 2012. Ecological transfer of radionuclides and metals to free-living earthworm species in natural habitats rich in NORM. Sci Total Environ. 414:167–176.
  • Müller W-U, Streffer C, Wojcik A, Niedereichholz F. 1999. Radiation-induced malformations after exposure of murin germ cells in various stages of spermatogenesis. Mutat Res. 425(1):99–106.
  • Nasulewicz A, Mazur A, Opolski A. 2004. Role of copper in tumour angiogenesis-clinical implications. J Trace Elem Med Biol. 18(1):1–8.
  • Pyle GG, Kamunde CN, McDonald DG, Wood CM. 2003. Dietary sodium inhibits aqueous copper uptake in rainbow trout (Oncorhynchus mykiss). J Exp Biol. 206(Pt 3):609–618.
  • Rades D, Lang S, Schild SE, Alberti W. 2006. Prognostic value of haemoglobin levels during concurrent radio-chemotherapy in the treatment of oesophageal cancer. Clin Oncol. 18(2):139–144.
  • Roh J-L, Park JY, Kim EH, Jang HJ, Kwon M. 2016. Activation of mitochondrial oxidation by PDK2 inhibition reverses cisplatin resistance in head and neck cancer. Cancer Lett. 371(1):20–29.
  • Salbu B, Denbeigh J, Smith RW, Heier LS, Teien HC, Rosseland BO, Oughton D, Seymour CB, Mothersill C. 2008. Environmentally relevant mixed exposures to radiation and heavy metals induce measurable stress responses in Atlantic salmon. Environ Sci Technol. 42(9):3441–3446.
  • Saroya R, Smith R, Seymour C, Mothersill C. 2010. Injection of reserpine into zebrafish prevents fish to fish communication of radiation-induced bystander signals: confirmation in vivo of a role for serotonin in the mechanism. Dose Response. 8:317–330.
  • Singh P. 2007. Role of Annexin-II in GI cancers: interaction with gastrins/progastrins. Cancer Lett. 252(1):19–35.
  • Sloman KA, Morgan TP, McDonald DG, Wood CM. 2003. Socially-induced changes in sodium regulation affect the uptake of water-borne copper and silver in rainbow trout, Oncorhynchus mykiss. Comparat Biochem Physiol C. 135(4):393–403.
  • Smith R, Wang J, Seymour C, Fernandez-Palomo C, Fazzari J, Schültke E, Bräuer-Krisch E, Laissue J, Schroll C, Mothersill C. 2018. Homogenous and microbeam X-ray radiation induces proteomic changes in the brains of irradiated rats and in the brains of non-irradiated cage mate rats. Dose Response. 16(1):1559325817750068.
  • Smith RW, Moccia RD, Mothersill CE, Seymour CB. 2018. Irradiation of rainbow trout at early life stages results in a proteomic legacy in adult gills. Part B; the effect of a second radiation dose, after one year, on the proteomic responses in the irradiated and non-irradiated bystander fish. Environ Res. 163:307–313.
  • Smith RW, Moccia RD, Seymour CB, Mothersill CE. 2018. Irradiation of rainbow trout at early life stages results in a proteomic legacy in adult gills. Part A; proteomic responses in the irradiated fish and in non-irradiated bystander fish. Environ Res. 163:297–306.
  • Smith RW, Saroya R, Seymour CB, Moccia RD, Mothersill CE. 2015. Exposure to acute levels of waterborne aluminium modifies the legacy of early life stage irradiation, including the communication of radiation-induced bystander signals, in adult rainbow trout. Int J Radiat Biol. 91(11):878–890.
  • Smith RW, Seymour CB, Moccia RD, Hinton TG, Mothersill CE. 2013. The induction of a radiation-induced bystander effect in fish transcends taxonomic group and trophic level. Int J Radiat Biol. 89(4):225–233.
  • Smith RW, Seymour CB, Moccia RD, Mothersill CE. 2015. Tissue-specific effects of acute aluminium exposure on the radiation-induced bystander effect in rainbow trout (Onchorynchus mykiss, Walbaum). Int J Radiat Biol. 91(9):715–723.
  • Smith RW, Seymour CB, Moccia RD, Mothersill CE. 2016. Irradiation of rainbow trout at early life stages results in trans-generational effects including the induction of a bystander effect in non-irradiated fish. Environ Res. 145:26–38.
  • Smith RW, Seymour CB, Mothersill CE. 2013. Short and long term bystander effect induction by fathead minnows (Pimphales promelas, Rafinesque, 1820) injected with environmentally relevant whole body doses of 226Ra. J Environ Radioact. 126:133–136.
  • Smith RW, Wang J, Bucking CP, Mothersill CE, Seymour CB. 2007. Evidence for a protective response by the gill proteome of rainbow trout exposed to X-ray induced bystander signals. Proteomics. 7(22):4171–4180.
  • Smith RW, Wang J, Mothersill CE, Hinton TG, Aizawa K, Seymour CB. 2011. Proteomic changes in the gills of wild-type and transgenic radiosensitive medaka following exposure to direct irradiation and to X-ray induced bystander signals. Biochim Biophys Acta. 1814(2):290–298.
  • Streffer C, Müller W-U. 1996. Malformations after radiation exposure of preimplantation stages. International Journal of Biology. 40:355–360.
  • Sun B, Gao L, Ahsan A, Chu P, Song Y, Li H, Zhang Z, Lin Y, Peng J, Song Z, et al. 2016. Anticancer effect of SZC015 on lung cancer cells through ROS-dependent apoptosis and autophagy induction mechanisms in vitro . Int Immunopharmacol. 40:400–409.
  • Valko M, Morris H, Cronin MT. 2005. Metals, toxicity and oxidative stress. Curr Med Chem. 12(10):1161–1208.
  • Wang N-N, Wang L-H, Li Y, Fu S-Y, Xue X, Jia L-N, Yuan X-Z, Wang Y-T, Tang X, Yang J-Y, et al. 2018. Targeting ALDH2 with disulfiram/copper reverses the resistance of cancer cells to microtubule inhibitors. Exp Cell Res. 362(1):72–82.
  • Wendelaar Bonga SE, Lock RAC. 1991. Toxicants and osmoregulation in fish. Neth J Zool. 42(2-3):478–493.
  • Yun S-L, Kim HH, Yoon JH, Park WS, Hahn M-J, Kim HC, Chung CH, Kim KK. 2015. Ubiquitin specific protease 4 positively regulates the WNT/β-catenin signaling in colorectal cancer. Mol Oncol. 9(9):1834–1851.
  • Zhang S, Li T, Zhang Y, Xu H, Li Y, Zi X, Yu H, Li J, Jin C-Y, Liu H-M. 2016. A new brominated chalcone derivative suppresses the growth of gastric cancer cells in vitro and in vivo involving ROS mediated up-regulation of DR5 and 4 expression and apoptosis . Toxicol Appl Pharmacol. 309:77–86.

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