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

References

• Alonzo F, Gilbin R, Zeman FA, Garnier-Laplace J. 2008. Increased effects of internal alpha irradiation in Daphnia magna after chronic exposure over three successive generation. Aquatic Toxicol 87:146–156.
   PubMed Web of Science ®Google Scholar
• Benjamin SA, Saunders WJ, Angleton GM, Lee AC. 1991. Radiation carcinogenesis in dogs irradiated during prenatal and postnatal development. Radiat Res 32:86–103.
   Web of Science ®Google Scholar
• Brent RL. 2014. Carcinogenic risks of prenatal ionizing radiation. Semin Fetal and Neonatal Med 19:203–213.
   PubMed Web of Science ®Google Scholar
• Calabrese EJ, Blain RB. 2011. The hormesis database: The occurrence of hormetic dose responses in the toxicological literature. Regulat Toxicol Pharmacol 61:73–81.
   PubMed Web of Science ®Google Scholar
• Calabrese EJ, Stanek EJ III, Nascarella MA. 2011. Evidence for hormesis in mutagenicity dose-response relationships. Mutat Res 726:91–97.
   PubMed Web of Science ®Google Scholar
• Camargo MMP, Fernandes MN, Martinez CBR. 2009. How aluminium exposure promotes osmoregulatory disturbances in the neotropical freshwater fish Prochilodus lineatus. Aquatic Toxicol 94:40–46.
   PubMed Web of Science ®Google Scholar
• Caplat C, Oral R, Mahaut M-L, Mao A, Barillier D, Guida M, Della Rocca C, Pagano G. 2010. Comparative toxicities of aluminum and zinc from sacrificial anodes or from sulfate salt in sea urchin embryos and sperm. Ecotoxicol Environ Safety 73:1138–1143.
   PubMed Web of Science ®Google Scholar
• Clutton SM, Townsend KM, Walker C, Ansell JD, Wright EG. 1996. Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis 17:1633–1639.
   PubMed Web of Science ®Google Scholar
• García-Medina S, Núñez-Betancourt JA, García-Medina AL, Galar-Martínez M, Neri-Cruz N, Islas-Flores H, Gómez-Oliván M. 2013. The relationship of cytotoxic and genotoxic damage with blood aluminum levels and oxidative stress induced by this metal in common carp (Cyprinus carpio). Ecotoxicol Environ Safety 96:191–197.
   PubMed Web of Science ®Google Scholar
• Guibaud G, Gauthier C. 2003. Study of aluminium concentrations and speciation of surface waters in four catchments in the Limousin region (France). J Inorganic Chem 97:16–25.
   PubMed Web of Science ®Google Scholar
• Griffioen KJS, Ghribi O, Savory J, DeWitt DA. 2004. Aluminum maltolate-induced toxicity in NT2 cells occurs through apoptosis and included cytochrome c release. Neurotoxicology 25:859–867.
   PubMed Web of Science ®Google Scholar
• Hornhardt S, Gomolka M, Walsh L, Jung T. 2006. Comparative investigations of sodium arsenite, arsenic trioxide and cadmium sulphate in combination with gamma-radiation on apoptosis, micronuclei induction and DNA damage in a human lymphoblastoid cell line. Mutat Res 600:165–176.
   PubMed Web of Science ®Google Scholar
• Kadhim MA, Macdonald DA, Goodhead DT, Lorimore SA, Marsden SJ, Wright EG. 1992. Transmission of chromosomal instability after plutonium alpha-particle irradiation. Nature 20;355(6362):738–740.
   PubMed Web of Science ®Google Scholar
• Kadhim MA, Moore SE, Goodwin EH. 2004. Review. Interrelationships amongst radiation-induced genomic instability, bystander effects and the adaptive response. Mutat Res 568:21–32.
   PubMed Web of Science ®Google Scholar
• Lankoff A, Banasik A, Duma A, Ochniak E, Lisowska H, Kuszewski T, Góźdź S, Wojcik A. 2006. A comet assay study reveals that aluminium induces DNA damage and inhibits the repair of radiation-induced lesions in human peripheral blood lymphocytes. Toxicol Lett 161:27–36.
   PubMed Web of Science ®Google Scholar
• Limoli CL, Ponnaiya B, Corcoran JJ, Giedzinski E, Kaplan MI, Hartmann A, Morgan WF. 2000. Genomic instability induced by high and low LET ionizing radiation. Adv Space Res 25:2107–2117.
   PubMed Web of Science ®Google Scholar
• Lyng FM, Seymour CB, Mothersill C. 2001. Oxidative stress in cells exposed to low levels of ionizing radiation. Biochem Soc Transact 29(Pt 2):350–353.
   PubMed Web of Science ®Google Scholar
• Macías G, Marco A, Blaustein AR. 2007. Combined exposure to ambient UVB and nitrite negatively affects survival of amphibian early life stages. Sci Total Environ 385:55–65.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Seymour C. 1997. Review. Lethal mutations and genomic instability. Int J Radiat Biol 71:751–758.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Seymour CB. 2004. Radiation-induced bystander effects – implications for cancer: A review. Nature Rev Cancer 4:158–164.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Bucking C, Smith RW, Agnihotri N, O’Neill A, Kilmade M, Seymour CB. 2006. Communication of radiation-induced bystander signals between fish in vivo. Environ Sci Technol 40:6859–6864.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Smith RW, Agnihotri N, Seymour CB. 2007. Characterization of a radiation-induced stress response in vivo between zebrafish. Environ Sci Technol 41:3382–3387.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Smith RW, Hinton TG, Aizawa K, Seymour CB. 2009. Communication of radiation-induced bystander signals in vivo between DNA deficient and proficient medaka (Oryzias latipes). Environ Sci Technol 43:3335–3342.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Smith RW, Saroya R, Denbeight 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 86:817–828.
   PubMed Web of Science ®Google Scholar
• 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 88:583–591.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Smith RW, Heier LS, Teien H-C, 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 irradiation. Radiat Environ Biophys 53:103–114.
   PubMed Web of Science ®Google Scholar
• Olsvik PA, Heier LS, Rosseland BO, Teien HC, Salbu B. 2010. Effects of combined γ-irradiation and metal (Al + Cd) exposures on Atlantic salmon (Salmo salar L.). J Environ Radioactivity 101:230–236.
   PubMed Web of Science ®Google Scholar
• O’Reilly S, Mothersill C, Seymour CB. 1994. Postirradiation expression of lethal mutations in an immortalized human keratinocyte cell line. Int J Radiat Biol 66:77–83.
   PubMed Web of Science ®Google Scholar
• Pereira S, Cavalie I, Camilleri V, Gilbin R, Adam-Guillermin C. 2013. Comparative genotoxicity of aluminum and cadmium in embryonic zebrafish cells. Mutat Res 750:19–26.
   PubMed Web of Science ®Google Scholar
• Prise KM, Folkard M, Michael BD. 2006. A review of the bystander effect and its implications for low-dose exposure. Radiat Protect Dosimetry 104:347–355.
   Google Scholar
• 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 stress responses in Atlantic salmon. Environ Sci Technol 42:3441–3446.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• Savory J, Herman MM, Ghribi O. 2003. Focused review. Intracellular mechanisms underlying aluminum-induced apoptosis in rabbit brain. J Inorganic Biochem 97:151–154.
   PubMed Web of Science ®Google Scholar
• Seymour CB, Mothersill C, Alper T. 1986. High yields of lethal mutations in somatic mammalian cells that survive ionizing radiation. Int J Radiat Biol Related Stud Phys, Chem Med 50:167–179.
   PubMed Web of Science ®Google Scholar
• Smith RW, Mothersill C, Honton T, Seymour CB. 2011. Exposure to low level chronic radiation leads to adaptation to a subsequent acute X-ray dose and communication of modified acute X-ray induced bystander signals in medaka (Japanese rice fish, Oryzias latipes). Int J Radiat Biol 87:1011–1022.
   PubMed Web of Science ®Google Scholar
• Smith RW, Seymour CB, Moccia RD, Hinton TG, Mothersill CE. 2013a. The induction of a radiation-induced bystander effect in fish transcends taxonomic group and trophic level. Int J Radiat Biol 89:225–233.
   PubMed Web of Science ®Google Scholar
• Smith RW, Seymour CB, Mothersill CE. 2013b. Short and long term bystander effect induction by fathead minnows (Pimephales promelas, Rafinesque, 1820) injected with environmentally relevant whole body doses of 226Ra J Env Radioactivity 126:133–136.
   Google Scholar
• Vanhoudt N, Vandenhove H, Real A, Bradshaw C, Stark K. 2012. A review of multiple stressor studies that include ionising radiation. Environ Pollut 168:177–192.
   PubMed Web of Science ®Google Scholar
• Vuorinen M, Vuorinen P, Hoikka J, Peuranen S. 1993. Lethal and sublethal threshold values of aluminium and acidity to pike (Esox lucius), whitefish (Coregonus lavaretus pallasi), pike perch (Stizostedion lucioperca) and roach (Rutilus rutilus) yolk-sac fry. Sci Total Environ 134(Suppl. 2):953–967.
   Google Scholar
• Watson GE, Lorimore SA, Macdonald DA, Wright EG. 2000. Chromosomal instability in unirradiated cells induced in vivo by a bystander effect of ionizing radiation. Cancer Res 60:5608–5611.
   PubMed Web of Science ®Google Scholar
• Zeng K-W, Fu H, Liu G-X, Wang X-M. 2012. Aluminum maltolate induced primary rat astrocyte apoptosis via overactivation of the class III P13K/Beclin 1-dependent autophagy signal. Toxicol In Vitro 26:215–220.
   PubMed Web of Science ®Google Scholar