Abstract
Multiple interactions between different pollutants in the surface waters can cause unpredictable consequences. The aim of the study was to evaluate the combined effect of two widespread xenobiotics, titanium oxide nanoparticles (TiO2) and bisphenol A (BPA), on freshwater bivalve Unio tumidus. The specimens were exposed for 14 days to TiCl4 (Ti, 1.25 µM), TiO2 (1.25 μM), BPA (0.88 nM), or their combination (TiO2 + BPA). Every type of exposure resulted in a particular oxidative stress response: TiO2 had antioxidant effect, decreasing the generation of reactive oxygen species (ROS) and phenoloxidase (PhO) activity, and doubling reduced glutathione (GSH) concentration in the digestive gland; Ti caused oxidative changes by increasing levels of ROS, PhO and superoxide dismutase; BPA decreased the GSH level by a factor of two. In the co-exposure treatment, these indices as well as lysosomal membrane stability were not affected. All Ti-containing exposures caused elevated levels of metalated metallothionein (Zn,Cu-MT), its ratio to total metallothionein protein, and lactate/pyruvate ratio. Both BPA-containing exposures decreased caspase-3 activity. All exposures, and particularly co-exposure, up-regulated CYP450-dependent oxidation, lipid peroxidation and lipofuscin accumulation, lysosomal cathepsin D and its efflux, as well as alkali-labile phosphates in gonads and caused DNA instability (except for TiO2). To summarize, co-exposure to TiO2 + BPA produced an overlap of certain individual responses but strengthened the damage. Development of water purification technologies using TiO2 requires further studies of the biological effects of its mixtures. U. tumidus can serve as a sentinel organism in such studies.
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Data availability
All data analyzed during this study are available via the Mendeley Data (https://doi.org/10.17632/cnhjzb2x49.1).
References
Aarab N, Lemaire-Gony S, Unruh E, Hansen PD, Larsen BK, Andersen OK, Narbonne JF (2006) Preliminary study of responses in mussel (Mytilus edilus) exposed to bisphenol A, diallyl phthalate and tetrabromodiphenyl ether. Aquat Toxicol 78:86–92. https://doi.org/10.1016/j.aquatox.2006.02.021
Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their use as biomarkers. Aquat Toxicol 76:160–202. https://doi.org/10.1016/j.aquatox.2005.08.015
Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113:548–555
Balbi T, Ciacci C, Grasselli E, Smerilli A, Voci A, Canesi L (2017) Utilization of Mytilus digestive gland cells for the in vitro screening of potential metabolic disruptors in aquatic invertebrates. Comp Biochem Physiol C 191:26–35. https://doi.org/10.1016/j.cbpc.2016.08.009
Banni M, Sforzini S, Balbi T, Corsi I, Viarengo A, Canesi L (2016) Combined effects of n-TiO2 and 2,3,7,8-TCDD in Mytilus galloprovincialis digestive gland: a transcriptomic and immunohistochemical study. Environ Res 145:135–144. https://doi.org/10.1016/j.envres.2015.12.003
Barmo C, Ciacci C, Canonico B, Fabbri R, Cortese K, Balbi T, Marcomini A, Pojana G, Gallo G, Canesi L (2013) In vivo effects of n-TiO2 on digestive gland and immune function of the marine bivalve Mytilus galloprovincialis. Aquat Toxicol 132–133:9–18. https://doi.org/10.1016/j.aquatox.2013.01.014
Baun A, Hartmann NB, Grieger K, Kusk KO (2008) Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing. Ecotoxicology 17(5):387–395. https://doi.org/10.1007/s10646-008-0208-y
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Benes P, Vetvicka V, Fusek M (2008) Cathepsin D—many functions of one aspartic protease. Crit Rev Oncol Hematol 68:12–28. https://doi.org/10.1016/j.critrevonc.2008.02.008
Bester MJ, Potgieter HC, Vermaak WJ (1994) Cholate and pH reduce interference by sodium dodecyl sulfate in the determination of DNA with Hoechst. Anal Biochem 223:299–305
Binelli A, Cogni D, Parolini M, Riva C, Provini A (2009) In vivo experiments for the evaluation of genotoxic and cytotoxic effects of Triclosan in Zebra mussel hemocytes. Aquat Toxicol 91:238–244. https://doi.org/10.1016/j.aquatox.2008.11.008
Bonomini M, Dottori S, Amoroso A, Arduini A, Sirolli V (2004) Increased platelet phosphatidylserine exposure and caspase activation in chronic uremia. J Thromb Haemost 2:1275–1281. https://doi.org/10.1111/j.1538-7836.2004.00837.x
Borys J, Maciejczyk M, Antonowicz B, Krętowski A, Waszkiel D, Bortnik P, Czarniecka-Bargłowska K, Kocisz M, Szulimowska J, Czajkowski M, Waszkiewicz N, Zalewska A (2018) Exposure to Ti4Al4V titanium alloy leads to redox abnormalities, oxidative stress, and oxidative damage in patients treated for mandible fractures. Oxid Med Cell Longev 2018:3714725. https://doi.org/10.1155/2018/3714725
Botta C, Labille J, Auffan M, Borschneck D, Miche H, Cabie M, Masion A, Rose J, Bottero JY (2011) TiO2-based nanoparticles released in water from commercialized sunscreens in a life-cycle perspective: structures and quantities. Environ Pollut 159:1543–1550. https://doi.org/10.1016/j.envpol.2011.03.003
Canesi L, Borghi C, Ciacci C, Fabbri R, Vergani L, Gallo G (2007) Bisphenol-A alters gene expression and functional parameters in molluscan hepatopancreas. Mol Cell Endocrinol 276(1–2):36–44. https://doi.org/10.1016/j.mce.2007.06.002
Canesi L, Corsi I (2016) Effects of nanomaterials on marine invertebrates. Sci Total Environ 565:933–940. https://doi.org/10.1016/j.scitotenv.2016.01.085
Canesi L, Frenzilli G, Balbi T, Bernardeschi M, Ciacci C, Corsolini S, DellaTorre C, Fabbri R, Faleri C, Focardi S, Guidi P, Kočan A, Marcomini A, Mariottini M, Nigro M, Pozo-Gallardo K, Rocco L, Scarcelli V, Smerilli A, Corsi I (2014) Interactive effects of n-TiO2 and 2,3,7,8-TCDD on the marine bivalve Mytilus galloprovincialis. Aquat Toxicol 153:53–65. https://doi.org/10.1016/j.aquatox.2013.11.002
Cavalieri EL, Rogan EG (2010) Is bisphenol A a weak carcinogen like the natural estrogens and diethylstilbestrol? IUBMB Life 62:746–751. https://doi.org/10.1002/iub.376
Chen X, Mao SS (2007) Titanium dioxide nanomaterials: synthesis, properties, modifications, and applications. Chem Rev 107:2891–2959. https://doi.org/10.1021/cr0500535
Christian P, Von der Kammer F, Baalousha M, Hofmann T (2008) Nanoparticles: structure, properties, preparation and behaviour in environmental media. Ecotoxicology 17(5):326–343. https://doi.org/10.1007/s10646-008-0213-1
Cinti DL, Moldeus P, Schenkman JB (1972) Kinetic parameters of drug metabolizing enzymes in Ca2+-sedimented microsomes from rat liver. Biochem Pharm 21:3249–3256. https://doi.org/10.1016/0006-2952(72)90089-5
Crain DA, Eriksen M, Iguchi T, Jobling S, Laufer H, Le Blanc GA, Guillette LJJ (2007) An ecological assessment of bisphenol-A: evidence from comparative biology. Reprod Toxicol 24:225–239. https://doi.org/10.1016/j.reprotox.2007.05.008
D’Agata A, Fasulo S, Dallas LJ, Fisher AS, Maisano M, Readman JW, Jha AN (2014) Enhanced toxicity of ‘bulk’ titanium dioxide compared to ‘fresh’ and ‘aged’ nano-TiO2 in marine mussels. Nanotoxicology 8:549–558. https://doi.org/10.3109/17435390.2013.807446
Della Torre C, Balbi T, Grassi G, Frenzilli G, Bernardeschi M, Smerilli A, Guidi P, Canesi L, Nigro M, Monaci F, Scarcelli V (2015) Titanium dioxide nanoparticles modulate the toxicological response to cadmium in the gills of Mytilus galloprovincialis. J Hazard Mater 297:92–100. https://doi.org/10.1016/j.jhazmat.2015.04.072
Dingle JT, Barrett AJ, Weston PD (1971) Cathepsin D. Characteristics of immunoinhibition and the confirmation of a role in cartilage breakdown. Biochem J 123:1–13. https://doi.org/10.1042/bj1230001
Diniz MS, de Matos AP, Lourenço J, Castro L, Peres I, Mendonça E, Picado A (2013) Liver alterations in two freshwater fish species (Carassius auratus and Danio rerio) following exposure to different TiO2 nanoparticle concentrations. Microsc Micro 19:1131–1140. https://doi.org/10.1017/S1431927613013238
Doyle JJ, Ward JE, Mason R (2016) Exposure of bivalve shellfish to titania nanoparticles under an environmental-spill scenario: encounter, ingestion and egestion. J Mar Biol Assoc UK 96:137–149. https://doi.org/10.1017/S0025315415001174.
Duncan KE, Ngu TT, Chan J, Salgado MT, Merrifield ME, Stillman MJ (2006) Peptide folding, metal-binding mechanisms, and binding site structures in metallothioneins. Exp Biol Med 231:1488–1499. https://doi.org/10.1177/153537020623100907
El-Said KS, Ali EM, Kanehira K, Taniguchi A (2014) Molecular mechanism of DNA damage induced by titanium dioxide nanoparticles in toll-like receptor 3 or 4 expressing human hepatocarcinoma cell lines. J Nanobiotechnol 12:48. https://doi.org/10.1186/s12951-014-0048-2
Falfushynska H, Gnatyshyna L, Ivanina A, Sokolova I, Stoliar O (2018) Detoxification and cellular stress responses of unionid mussels Unio tumidus from two cooling ponds to combined nano-ZnO and temperature stress. Chemosphere 193:1127–1142. https://doi.org/10.1016/j.chemosphere.2017.11.079
Falfushynska H, Gnatyshyna L, Yurchak I, Sokolova I, Stoliar O (2015) The effects of zinc nanooxide on cellular stress responses of the freshwater mussels Unio tumidus are modulated by elevated temperature and organic pollutants. Aquat Toxicol 162:82–93. https://doi.org/10.1016/j.aquatox.2015.03.006
Falfushynska HI, Delahaut L, Stolyar OB, Geffard A, Biagianti-Risbourg S (2009) Multi-biomarkers approach in different organs of Anodonta cygnea from the Dnister Basin (Ukraine). Arch Environ Contam Toxicol 57:86–95. https://doi.org/10.1007/s00244-008-9234-2
Fang T, Yu LP, Zhang WC, Bao SP (2015) Effects of humic acid and ionic strength on TiO2 nanoparticles sublethal toxicity to zebrafish. Ecotoxicology 24(10):2054–2066. https://doi.org/10.1007/s10646-015-1541-6
Federici G, Shaw BJ, Handy RD (2007) Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84:415–430. https://doi.org/10.1016/j.aquatox.2007.07.009
Fu PP, Xia Q, Hwang HM, Ray PC, Yu H (2014) Mechanisms of nanotoxicity: generation of reactive oxygen species. J Food Drug Anal 22:64–75. https://doi.org/10.1016/j.jfda.2014.01.005
Gagné F, André C (2011) New approaches to indirect vitellogenin-like protein evaluations in aquatic oviparous and ovoviviparous organisms. Fresen Environ Bull 20:12–17
Gagné F, Blaise C, Pellerin J, Pelletier E, Douville M, Gauthier-Clerc S, Viglino L (2003) Sex alteration in soft-shell clams (Mya arenaria) in an intertidal zone of the Saint Lawrence River (Quebec, Canada). Comp Biochem Physiol C 134:189–198. https://doi.org/10.1016/S1532-0456(02)00248-X
Gassman NR (2017) Induction of oxidative stress by bisphenol A and its pleiotropic effects. Environ Mol Mutagen 58:60–71. https://doi.org/10.1002/em.22072
Gawehn K (1988) D-(-)-Lactate. Іn: Bergmeyer HU (еd.) Methods of enzymatic analysis, vol. VI, 3rd edn. VCH Publishers (UK) Ltd., Cambridge, UK, pp. 588–592
Geiseler B, Miljevic M, Müller P, Fruk L (2012) Phototriggered production of reactive oxygen species by TiO2 nanospheres and rods. J Nanomater 2012:1–9. https://doi.org/10.1155/2012/708519
Geist J (2011) Integrative freshwater ecology and biodiversity conservation. Ecol Indic 11:1507–1516. https://doi.org/10.1016/j.ecolind.2011.04.002
Giese B, Klaessig F, Park B, Kaegi R, Wigger MH, von Gleich A, Gottschalk F (2018) Risks, release and concentrations of engineered nanomaterial in the environment. Sci Rep 8:1565. https://doi.org/10.1038/s41598-018-19275-4
Gondikas A, von der Kammer F, Kaegi R, Borovinskaya O, Neubauer E, Navratilova J, Praetorius A, Cornelis G, Hofmann T (2018) Where is the nano? Analytical approaches for the detection and quantification of TiO2 engineered nanoparticles in surface waters. Environ Sci: Nano 5:313–326. https://doi.org/10.1039/C7EN00952F
Guo Y, Chen L, Wu J, Hua J, Yang L, Wang Q, Zhang W, Lee JS, Zhou B (2019) Parental co-exposure to bisphenol A and nano-TiO2 causes thyroid endocrine disruption and developmental neurotoxicity in zebrafish offspring. Sci Total Environ 650(1):557–565. https://doi.org/10.1016/j.scitotenv.2018.09.007
Heinlaan M, Ivask A, Blinova I, Dubourguier HC, Kahru A (2008) Toxicity of nanosized and bulk ZnO, CuO and TiO2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere 71:1308–1316. https://doi.org/10.1016/j.chemosphere.2007.11.047
Ike M, Jin CS, Fujita M (2000) Biodegradation of bisphenol A in the aquatic environment. Water Sci Technol 42(7–8):31–38. https://doi.org/10.2166/wst.2000.0549
Khalilova HK, Hasanova SA, Aliyev FG (2018) Photocatalytic removal of organic pollutants from industrial wastewater using TiO2 catalyst. J Environ Prot 9:691–698. https://doi.org/10.4236/jep.2018.96043
Khene L, Berrebbah H, Yahyaoui A, Bouarroudj T, Zouainia S, Kahli H, Bourayou C (2017) Biomarkers of oxidative stress, lipid peroxidation and ROS production induced by TiO2 microparticles on snails Helix aspersa. Stud Univ “Vasile Goldiş” 27:127–133
Kim KT, Eo MY, Nguyen TTH, Kim SM (2019) General review of titanium toxicity. Int J Implant Dent 5:10. https://doi.org/10.1186/s40729-019-0162-x
Klotz AV, Stegeman JJ, Walsh C (1984) An alternative 7-ethoxyresorufin O-deethylase activity assay: a continuous visible spectrophotometric method for measurement of cytochrome P-450 monooxygenase activity. Anal Biochem 140:138–145
Krezel A, Maret W (2007) Different redox states of metallothionein/thionein in biological tissue. Biochem J 402:551–558. https://doi.org/10.1042/BJ20061044
Lee BC, Kim S, Shon HK, Vigneswaran S, Kim SD, Cho J, Kim IS, Choi KH, Kim JB, Park HJ, Kim JH (2009) Aquatic toxicity evaluation of TiO2 nanoparticle produced from sludge of TiCl4 flocculation of wastewater and seawater. J Nanopart Res 11:2087–2096. https://doi.org/10.1007/s11051-008-9574-x
Li L, Sillanpää M, Risto M (2016) Influences of water properties on the aggregation and deposition of engineered titanium dioxide nanoparticles in natural waters. Environ Pollut 219:132–138. https://doi.org/10.1016/j.envpol.2016.09.080
Lopes-Lima M, Sousa R, Geist J, Aldridge DC, Araujo R, Bergengren J, Bespalaya Y, Bódis E, Burlakova L, Van Damme D, Douda K, Froufe E, Georgiev D, Gumpinger C, Karatayev A, Kebapçi Ü, Killeen I, Lajtner J, Larsen BM, Lauceri R, Legakis A, Lois S, Lundberg S, Moorkens E, Motte G, Nagel KO, Ondina P, Outeiro A, Paunovic M, Prié V, von Proschwitz T, Riccardi N, Rudzīte M, Rudzītis M, Scheder C, Seddon M, Şereflişan H, Simić V, Sokolova S, Stoeckl K, Taskinen J, Teixeira A, Thielen F, Trichkova T, Varandas S, Vicentini H, Zajac K, Zajac T, Zogaris S (2017) Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biol Rev 92:572–607. https://doi.org/10.1111/brv.12244
Lowry OH, Rosebroungh HJ, Farr AL, Randall RJ (1951) Protein measurement with Folin phenol reagent. J Biol Chem 191:265–275
Lu N, Lu Y, Liu F, Zhao K, Yuan X, Zhao Y, Li Y, Qin H, Zu J (2013) H3PW12O40/TiO2 catalyst-induced photodegradation of bisphenol A (BPA): kinetics, toxicity and degradation pathways. Chemosphere 91:1266–1272. https://doi.org/10.1016/j.chemosphere.2013.02.023
Luna-Acosta A, Thomas-Guyon H, Amar M, Rosenfeld E, Bustamante P, Fruitier-Arnaudin I (2011) Differential tissue distribution and specificity of phenoloxidases from the Pacific oyster Crassostrea gigas. Comp Biochem Physiol B 159:220–226. https://doi.org/10.1016/j.cbpb.2011.04.009
Lydeard C, Cowie RH, Ponder WF, Bogan AE, Bouchet P, Clark SA, Cummings KS, Frest TJ, Gargominy O, Herbert DG, Hershler R, Perez KE, Roth B, Seddon M, Strong EE, Thompson FG (2004) The global decline of nonmarine mollusks. BioScience 54:321–330. https://doi.org/10.1641/0006-3568(2004)054[0321:TGDONM]2.0.CO;2
Man SM, Kanneganti T-D (2016) Regulation of lysosomal dynamics and autophagy by CTSB/cathepsin B. Autophagy 12:2504–2505. https://doi.org/10.1080/15548627.2016.1239679
Manfrin C, De Moro G, Torbol V, Venier P, Pallavicini A, Gerdol M (2012) Physiological and molecular responses of bivalves to toxic dinoflagellates. ISJ 9:184–199
Manibabu PV, Patnaik BK (1997) Lipofuscin concentration of the brain shows a reduction with age in male garden lizard. Comp Biochem Physiol C 117:229–232. https://doi.org/10.1016/S0742-8413(97)00054-6
Marchi B, Burlando B, Moore MN, Viarengo A (2004) Mercury- and copper-induced lysosomal membrane destabilisation depends on [Ca2+] dependent phospholipase A2 activation. Aquat Toxicol 66:197–204. https://doi.org/10.1016/j.aquatox.2003.09.003
Minetto D, Libralato G, Volpi Ghirardini A (2014) Ecotoxicity of engineered TiO2 nanoparticles to saltwater organisms: an overview. Environ Int 66:18–27. https://doi.org/10.1016/j.envint.2014.01.012
Mischuk YV, Stoliar OB (2009) Peculiarities of metallothioneins of the bivalve mollusk Anodonta cygnea L. in the natural and laboratory living conditions. Hydrobiol J 45:63–71. https://doi.org/10.1615/HydrobJ.v45.i5.70
Moriyama A, Yamada I, Takahashi J, Iwahashi H (2018) Oxidative stress caused by TiO2 nanoparticles under UV irradiation is due to UV irradiation not through nanoparticles. Chem Biol Inter 294:144–150. https://doi.org/10.1016/j.cbi.2018.08.017
Oehlmann J, Schulte-Oehlmann U, Kloas W, Jagnytsch O, Lutz I, Kusk KO, Wollenberger L, Santos EM, Paull GC, Van Look KJ, Tyler CR (2009) A critical analysis of the biological impacts of plasticizers on wildlife. Philos Trans R Soc Lond B 364:2047–2062. https://doi.org/10.1098/rstb.2008.0242
Ohkawa H, Onishi N, Yagi K (1979) Assay for lipid peroxidation in animal tissue by thiobarbituric acid reaction. Anal Biochem 95:351–358. https://doi.org/10.1016/0003-2697(79)90738-3
Olive PL (1988) DNA precipitation assay: a rapid and simple method for detecting DNA damage in mammalian cells. Environ Mol Mutagen 11:487–495. https://doi.org/10.1002/em.2850110409
Petković J, Žegura B, Filipič M (2011) Influence of TiO2 nanoparticles on cellular antioxidant defense and its involvement in genotoxicity in HepG2 cells. J Phys Conf Ser 304:012037. https://doi.org/10.1088/1742-6596/304/1/012037
Ptak A, Rak-Mardyła A, Gregoraszczuk EL (2013) Cooperation of bisphenol A and leptin in inhibition of caspase-3 expression and activity in OVCAR-3 ovarian cancer cells. Toxicol Vitr 27:1937–1943. https://doi.org/10.1016/j.tiv.2013.06.017
Ranjan S, Dasgupta N, Sudandiradoss C, Ramalingam C, Kumar A (2018) Titanium dioxide nanoparticle-protein interaction explained by docking approach. Int J Nanomed 13(T-NANO 2014 Abstracts):47–50. https://doi.org/10.2147/IJN.S125008
Reeves JF, Davies SJ, Dodd NJ, Jha AN (2008) Hydroxyl radicals (OH) are associated with titanium dioxide (TiO2) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells. Mutat Res 640:113–122. https://doi.org/10.1016/j.mrfmmm.2007.12.010
Roesijadi G, Fowler BA (1991) Purification of invertebrate metallothioneins. Methods Enzym 205:263–273. https://doi.org/10.1016/0076-6879(91)05106-6
Rozes L, Steunou N, Fornasieri G, Sanchez C (2006) Titanium-oxo clusters, versatile nanobuilding blocks for the design of advanced hybrid materials. Mon Chem 137:501–528. https://doi.org/10.1007/s00706-006-0464-6
Rubin BS (2011) Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol 127:27–34. https://doi.org/10.1016/j.jsbmb.2011.05.002
Ruttkay-Nedecky B, Nejdl L, Gumulec J, Zitka O, Masarik M, Eckschlager T, Stiborova M, Adam V, Kizek R (2013) The role of metallothionein in oxidative stress. Int J Mol Sci 14:6044–6066. https://doi.org/10.3390/ijms14036044
Saìnchez-Marín P, Fernaìndez-Gonzaìlez LE, Mantilla-Aldana L, Diz AP, Beiras R (2017) Shotgun proteomics analysis discards alkali-labile phosphate as a reliable method to assess vitellogenin levels in Mytilus galloprovincialis. Environ Sci Technol 51:7572–7580. https://doi.org/10.1021/acs.est.7b01734
Scott AP (2013) Do mollusks use vertebrate sex steroids as reproductive hormones? II. Critical review of the evidence that steroids have biological effects. Steroids 78:268–281. https://doi.org/10.1016/j.steroids.2012.11.006
Siebert MN, Mattos JJ, Piazza CE, de Lima D, Gomes CHA, de Melo CM, Bainy AC (2017) Characterization of ethoxyresorufin O-deethylase activity (EROD) in oyster Crassostrea brasiliana. Comp Biochem Physiol B 203:115–121. https://doi.org/10.1016/j.cbpb.2016.10.002
Sies H (2015) Oxidative stress: a concept in redox biology and medicine. Redox Biol 4:180–183. https://doi.org/10.1016/j.redox.2015.01.002
Sun TY, Mitrano DM, Bornhöft NA, Scheringer M, Hungerbühler K, Nowack B (2017) Envisioning nano release dynamics in a changing world: using dynamic probabilistic modeling to assess future environmental emissions of engineered nanomaterials. Environ Sci Technol 51:2854–2863. https://doi.org/10.1021/acs.est.6b05702
Sureda A, Capó X, Busquets-Cortés C, Tejada S (2018) Acute exposure to sunscreen containing titanium induces an adaptive response and oxidative stress in Mytillus galloprovincialis. Ecotoxicol Environ Saf 149:58–63. https://doi.org/10.1016/j.ecoenv.2017.11.014
Sutherland DE, Summers KL, Stillman MJ (2012) Noncooperative metalation of metallothionein 1a and its isolated domains with zinc. Biochemistry 51:6690–6700. https://doi.org/10.1021/bi3004523
Trouiller B, Reliene R, Westbrook A, Solaimani P, Schiestl RH (2009) Titanium dioxide nanoparticles induce DNA damage and genetic instability in vivo in mice. Cancer Res 69:8784–8789. https://doi.org/10.1158/0008-5472.CAN-09-2496
Turk B, Stoka V (2007) Protease signalling in cell death: caspases versus cysteine cathepsins. FEBS Lett 581:2761–2767. https://doi.org/10.1016/j.febslet.2007.05.038
Unuma T, Sawaguchi S, Yamano K, Ohta H (2011) Accumulation of the major yolk protein and zinc in the agametogenic sea urchin gonad. Biol Bull 221:227–237. https://doi.org/10.1086/BBLv221n2p227
Ursini F, Maiorino M, Forman HJ (2016) Redox homeostasis: The Golden Mean of healthy living. Redox Biol 8:205–215. https://doi.org/10.1016/j.redox.2016.01.010
Viarengo A, Burlando B, Cavaletto M, Marchi B, Ponzano E, Blasco J (1999) Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. Am J Phys 277:R1612–R1619. https://doi.org/10.1152/ajpregu.1999.277.6.R1612
Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic Molluscs. Mar Environ Res 44:69–84. https://doi.org/10.1016/S0141-1136(96)00103-1
Wang J, Hou Y, Ma J (2013) Titanium(IV) intake by apotransferrin. In: Kretsinger RH, Uversky VN, Permyakov EA (еds) Encyclopedia of metalloproteins. Springer, New York, NY
Weber E (2005) Population size and structure of three mussel species (Bivalvia: Unionidae) in a northeastern German river with special regard to influences of environmental factors. Hydrobiologia 537:169–183. https://doi.org/10.1007/s10750-004-2839-1
Yang F, Zeng L, Luo Z, Wang Z, Huang F, Wang Q, Drobne D, Yan C (2018) Complex role of titanium dioxide nanoparticles in the trophic transfer of arsenic from Nannochloropsis maritima to Artemia salina nauplii. Aquat Toxicol 198:231–239. https://doi.org/10.1016/j.aquatox.2018.03.009
Zhang C, Lohwacharin J, Takizawa S (2017) Properties of residual titanium dioxide nanoparticles after extended periods of mixing and settling in synthetic and natural waters. Sci Rep 7:9943. https://doi.org/10.1038/s41598-017-09699-9
Zierden MR, Valentine AM (2016) Contemplating a role for titanium in organisms. Metallomics 8:9–16. https://doi.org/10.1039/c5mt00231a
Zoltan T, Rosales MC, Yadarola C (2016) Reactive oxygen species quantification and their correlation with the photocatalytic activity of TiO2 (anatase and rutile) sensitized with asymmetric porphyrins. J Environ Chem Eng 4:3967–3980. https://doi.org/10.1016/j.jece.2016.09.008
Acknowledgements
This work was funded by the grants from the Ministry of Education and Science of Ukraine for O. Stoliar (Projects M/4-2013; M/70-2017, 132B). We thank Dr. Sci. Olexandr Zaichenko and Dr. Sci. Natalia Mitina (Lviv Polytechnic National University, Ukraine) for their assistance with the physical–chemical characterization of the nanoparticles. The authors are grateful Dr. Inna Birchenko and Proof-Reading-Service.com for the scientific editing, linguistic and phraseological improvement of this manuscript.
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Gnatyshyna, L., Falfushynska, H., Horyn, O. et al. Biochemical responses of freshwater mussel Unio tumidus to titanium oxide nanoparticles, Bisphenol A, and their combination. Ecotoxicology 28, 923–937 (2019). https://doi.org/10.1007/s10646-019-02090-6
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DOI: https://doi.org/10.1007/s10646-019-02090-6