journal article·2014-04

The effect of titanium dioxide nanoparticles on antioxidant gene expression in tilapia (Oreochromis niloticus)

Ruth Varela-Valencia, Nikte Gómez-Ortiz, Gerko Oskam, Romeo de Coss, Jorge Rubio-Piña, Marcela del Río-García, Arnulfo Albores-Medina, Omar Zapata-Perez

Journal of Nanoparticle Research· Volume 16· Issue 4
Publisher page

Abstract

The reactivity of nanoparticles (NPs) in biological systems is well recognized, but there are huge gaps in our understanding of NP toxicity in fish, despite a number of recent ecotoxicity studies. Therefore, the aim of this research was to evaluate the effect of titanium dioxide NPs (TiO2-NPs) on antioxidant gene expression in the tilapia, Oreochromis niloticus. First, different sizes, shapes, and phases of TiO2-NPs were synthesized and characterized by scanning electron microscopy (SEM), X-ray diffraction (XRD), and dynamic light scattering (DLS). Fish were injected intraperitoneally with different concentrations (0.1, 1.0, 10.0 mg/L), sizes (7, 14, and 21 nm), and phases (anatase and rutile) of TiO2-NPs, and sacrificed 3, 6, 12, and 24 h after injection, when their livers were removed. Total RNA was extracted, and expression of the catalase (CAT), glutathione-S-transferase (GST), and superoxide dismutase (SOD) genes was assessed by real-time polymerase chain reaction (RT-PCR). The results showed that injection of 1.0 mg/L TiO2-NPs induced an initial mild increase in CAT, GST, and SOD gene expression in tilapia, after which transcript levels decreased. Fish injected with 7 and 14 nm TiO2-NPs showed an increase in antioxidant transcript levels 6 h after treatment. Finally, the rutile form generated stronger induction of the GST gene than anatase TiO2-NPs during the first 6 h after injection, which suggests that exposure to rutile causes higher levels of reactive oxygen species to be produced.
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OpenAlex topics: Nanoparticles: synthesis and applications · Environmental Toxicology and Ecotoxicology · Microplastics and Plastic Pollution

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References (69)

Show source-provided references
1. Aluja AS (2000) Animales de laboratorio y la Norma Oficial Mexicana (NOM-062-ZOO-1999). Gaceta Médica de México 138:17–24
2. Ballard CP, Fanelli AJ (1993) Sol-gel route for material synthesis. In: Rao CNR (ed) Chemistry of advanced materials. Blackwell Scientific Publications, London
3. Borm PJA, Robbins D, Haubold S, Kuhlbusch T, Fissan Heinz, Donaldson K, Schins R, Stone V, Kreyling W, Lademann J, Krutmann J, Warheit D, Oberdorster E (2006) The potential risks of nanomaterials: a review carried out for ECETOC. Part Fibre Toxicol 3:11. doi: 10.1186/1743-8977-3-1110.1186/1743-8977-3-11 ↗
4. Braydich-Stolle LK, Schaeublin NM, Murdock RC, Jiang J, Biswas P, John J, Saber MH (2009) Crystal structure mediates mode of cell death in TiO2 nanotoxicity. J Nanopart Res 11:1361–1374. doi: 10.1007/s11051-008-9523-810.1007/s11051-008-9523-8 ↗
5. Carinci F, Volinia S, Pezzetti F, Francioso F, Tosi L, Piattelli A (2003) Titanium-cell interaction: analysis of gene expression profiling. J Biomed Mater Res 66B:341–346. doi: 10.1002/jbm.b.1002110.1002/jbm.b.10021 ↗
6. Choi JS, Jun YW, Yeon SI, Kim HC, Shin JS, Cheon J (2006) Biocompatible heterostructured nanoparticles for multimodal biological detection. J Am Chem Soc 128:15982–15983. doi: 10.1186/1741-7015-8-8310.1021/ja066547g ↗
7. Crane M, Handy RD, Garrod J, Owen R (2008) Ecotoxicity test methods and environmental hazard assessment for engineered nanoparticles. Ecotoxicology 17:421–443. doi: 10.1007/s10646-008-0215-z10.1007/s10646-008-0215-z ↗
8. Cullity BD (1978) Elements of X-ray diffraction, 2nd edn. Addison-Wesley, Massachusetts
9. Emerich DF, Thanos CG (2003) Nanotechnology and medicine. Expert Opin Biol Therapy 3:655–663. doi: 10.1517/14712598.3.4.65510.1517/14712598.3.4.655 ↗
10. Eom HJ, Choi J (2009) Oxidative stress of CeO2 nanoparticles via p38-Nrf-2 signaling pathway in human bronchial epithelial cell, Beas-2B. Toxicol Lett 187:77–83. doi: 10.1016/j.toxlet.2009.01.02810.1016/j.toxlet.2009.01.028 ↗
11. Esterkin CR, Negro AC, Alfano OM, Cassano AE (2005) Air pollution remediation in a fixed bed photocatalytic reactor coated with TiO2. AIChE J 51:2298–2310. doi: 10.1002/aic.1047210.1002/aic.10472 ↗
12. Farré M, Gajda-Schrantz K, Kantiani L, Barceló D (2009) Ecotoxicity and analysis of nanomaterials in the aquatic environment. Anal Bioanal Chem 393:81–95. doi: 10.1007/s00216-008-2458-110.1007/s00216-008-2458-1 ↗
13. Federici G, Shaw BJ, Handy RD (2007) Toxicity of titanium dioxide nanoparticules to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84:415–430. doi: 10.1016/j.aquatox.2007.07.00910.1016/j.aquatox.2007.07.009 ↗
14. Ferin J, Oberdöster G (1985) Biological effects and toxicity assessment of titanium dioxides: anatase and rutile. Am Ind Hyg Assoc J 46:69–72. doi: 10.1080/1529866859139441910.1080/15298668591394419 ↗
15. Filho DW (1996) Fish antioxidant defenses—a comparative approach. Braz J Med Biol Res 29:1735–1742
16. Foster KA, Galeffi F, Gerich FJ, Turner DA, Muller M (2006) Optical and pharmacological tools to investigate the role of mitochondria during oxidative stress and neurodegeneration. Prog Neurobiol 79:136–171. doi: 10.1016/j.pneurobio.2006.07.00110.1016/j.pneurobio.2006.07.001 ↗
17. Green M, Howman E (2005) Semiconductor quantum dots and free radical induced DNA nicking. Chem Commun 121:121–123. doi: 10.1039/B413175D10.1039/b413175d ↗
18. Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27:1972–1978. doi: 10.1897/08-002.110.1897/08-002.1 ↗
19. Gurr JR, Wang ASS, Chen KCH, Jan Y (2005) Ultrafine titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells. Toxicology 213:66–73. doi: 10.1016/j.tox.2005.05.00710.1016/j.tox.2005.05.007 ↗
20. Hall S, Bradley T, Moore JT, Kuykindall T, Minella L (2009) Acute and chronic toxicity of nano-scale TiO2 particles to freshwater fish, cladocerans, and green algae, and effects of organic and inorganic substrate on TiO2 toxicity. Nanotoxicology 3:91–97. doi: 10.1080/1743539090278807810.1080/17435390902788078 ↗
21. Hao L, Wang Z, Xing B (2009) Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in Juvenile Carp (Cyprinus carpio). J Environ Sci 21:1459–1466. doi: 10.1016/S1001-0742(08)62440-710.1016/S1001-0742(08)62440-7 ↗
22. Hirakawa K, Mori M, Yoshida M, Oikawa S, Kawanishi S (2004) Photo-irradiated titanium dioxide catalyzes site specific DNA damage via generation of hydrogen peroxide. Free Radic Res 38:439–447. doi: 10.1080/107157604200020648710.1080/1071576042000206487 ↗
23. Hund-Rinke K, Simon M (2006) Ecotoxic Effect of photocatalytic active nanoparticles (TiO2) on algae and daphnids. Environ Sci Pollut Res 3:225–232. doi: 10.1065/espr2006.06.31110.1065/espr2006.06.311 ↗
24. Hussain N, Jaitley V, Florence AT (2001) Recent advances in the understanding of uptake of microparticulates across the gastrointestinal lymphatics. Adv Drug Deliv Rev 50:107–142. doi: 10.1016/j.tox.2009.04.00110.1016/S0169-409X(01)00152-1 ↗
25. Hussain S, Bolanda S, Baeza-Squibana A, Hamela R, Thomassen LCJ, Martens JA, Billon-Galland MA, Fleury-Feithd J, Moisan F, Pairon JC, Marano F (2009) Oxidative stress and proinflammatory effects of carbon black and titanium dioxide nanoparticles: role of particle surface area and internalized amount. Toxicology 260:142–149. doi: 10.1016/j.tox.2009.04.00110.1016/j.tox.2009.04.001 ↗
26. Jin C, Tang Y, Yang FG, Li XL, Xu S, Fan XY, Huang YY, Yang YJ (2011) Cellular toxicity of TiO2 nanoparticles in anatase and rutile crystal phase. Biol Trace Elem Res 141:3–15. doi: 10.1007/s12011-010-8707-010.1007/s12011-010-8707-0 ↗
27. Jovanovic B, Ji T, Palic D (2011) Gene expression of zebrafish embryos exposed to titanium dioxide nanoparticles and hydroxylated fullerenes. Ecotoxicol Environ Saf 6:1518–1525. doi: 10.1016/j.ecoenv.2011.04.01210.1016/j.ecoenv.2011.04.012 ↗
28. Kahru A, Dubourguier HC (2010) From ecotoxicology to nanoecotoxicology. Toxicology 269:105–119. doi: 10.1016/j.tox.2009.08.01610.1016/j.tox.2009.08.016 ↗
29. Kang JL, Moon C, Lee HS, Lee HW, Park EM, Kim HS, Castranova V (2008a) Comparison of the biological activity between ultrafine and fine titanium dioxide particles in RAW 264.7 cells associated with oxidative stress. J Toxicol Environ Health A 71:478–485. doi: 10.1080/1528739080190667510.1080/15287390801906675 ↗
30. Kang SJ, Kim BM, Lee YJ, Chung HW (2008b) Titanium dioxide nanoparticles trigger p53-mediated damage response in peripheral blood lymphocytes. Environ Mol Mutagen 49:399–405. doi: 10.1002/em.2039910.1002/em.20399 ↗
31. Kim KT, Klaine SJ, Cho J, Kim SH, Kim SD (2010) Oxidative stress responses of Daphnia magna exposed to TiO2 nanoparticles according to size fraction. Sci Total Environ 408:2268–2272. doi: 10.1016/j.scitotenv.2010.01.04110.1016/j.scitotenv.2010.01.041 ↗
32. Lam CW, James JT, McCluskey R, Hunter RL (2004) Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol Sci 77:126–134. doi: 10.1093/toxsci/kfg24310.1093/toxsci/kfg243 ↗
33. Limbach LK, Wick P, Manser P, Grass RN, Bruinink A, Stark WJ (2007) Exposure of engineered nanoparticles to human lung epithelial cells: influence of chemical composition and catalytic activity on oxidative stress. Environ Sci Technol 41:4158–4163. doi: 10.1021/es062629t10.1021/es062629t ↗
34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408. doi: 10.1006/meth.2001.126210.1006/meth.2001.1262 ↗
35. Long TC, Tajuba J, Sama P, Saleh N, Swartz C, Parker J, Hester S, Lowry GV, Veronesi B (2007) Nanosize titanium dioxide stimulates reactive oxygen species in brain microglia and damages neurons in vitro. Environ Health Perspect 115:1631–1637. doi: 10.1289/ehp.1021610.1289/ehp.10216 ↗
36. Lovern SB, Klaper R (2006) Daphnia magna mortality when exposed to titanium dioxide and fullerene (L60) nanoparticles. Environ Toxicol Chem 25:1132–1137. doi: 10.1897/05-278R.110.1897/05-278R.1 ↗
37. Matranga V, Corsi I (2012) Toxic effects of engineered nanoparticles in the marine environment: model organisms and molecular approaches. Mar Environ Res 76:32–40. doi: 10.1016/j.marenvres.2012.01.00610.1016/j.marenvres.2012.01.006 ↗
38. Muller NC, Nowack B (2008) Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453. doi: 10.1021/es702963710.1021/es7029637 ↗
39. Oberdörster E (2004) Manufactured nanomaterials (Fullerenes, C60) induce oxidative stress in the brain of juvenile largemouth bass. Environ Health Perspect 112:1058–1062. doi: 10.1289/ehp.702110.1289/ehp.7021 ↗
40. Oberdörster G, Ferin J, Gelein R, Soderholm SC, Finkelstein J (1992) Role of the alveolar macrophage in lung injury: studies with ultrafine particles. Environ Health Perspect 97:193–199. doi: 10.2307/343135310.1289/ehp.9297193 ↗
41. Oberdörster G, Oberdörster E, Oberdörster J (2005) Nanotoxicology: an emerging Discipline Evolving from studies of ultrafine particles. Environ Health Perspect 113:823–839. doi: 10.1289/ehp.733910.1289/ehp.7339 ↗
42. Oskam G, Nellore A, Penn RL, Searson PC (2003) The growth kinetics of TiO2 nanoparticles from titanium(IV) alkoxide at high water/titanium ratio. J Phys Chem B 8:1734–1738. doi: 10.1021/jp021237f10.1021/jp021237f ↗
43. Pandey S, Parvez S, Sayeed I, Haque R, Bin-Hafeez B, Raisuddin S (2003) Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago attu (Bl. & Schn.). Sci Total Environ 309:105–115. doi: 10.1016/j.bbr.2011.03.03110.1016/S0048-9697(03)00006-8 ↗
44. Park NG, Van de Lagemaat J, Frank AJ (2000) Comparison of dye-sensitized rutile- and anatase-based TiO2 solar cells. J Phys Chem B 104:8989–8994. doi: 10.1021/jp994365l10.1021/jp994365l ↗
45. Park EJ, Yi J, Chung KH, Ryu DY, Choi J, Park K (2008) Oxidative stress and apoptosis induced by titanium dioxide nanoparticles in cultured BEAS-2B cells. Toxicol Lett 180:222–229. doi: 10.1016/j.toxlet.2008.06.86910.1016/j.toxlet.2008.06.869 ↗
46. Patil VK, David M (2008) Behaviour and respiratory dysfunction as an index of malathion toxicity in the freshwater fish, Labeo rohita (Hamilton). Turkish J Fish Aquat Sci 8:233–237. doi: 10.3109/01480540903196816
47. Pérez S, Farré MI, Barceló D (2009) Analysis behavior and ecotoxicity of carbón-based nanomaterials in the aquatic environment. TrAC, Trends Anal Chem 28:820–832. doi: 10.1016/j.trac.2009.04.00110.1016/j.trac.2009.04.001 ↗
48. PICUAL-Cinvestav (2002) Programa Institucional para el Cuidado y Uso de los Animales de Laboratorio del Centro de Investigación y Estudios Avanzados del IPN
49. Powers KW, Brown SC, Krishna VB, Wasdo SC, Moudgil BM, Roberts SM (2006) Research strategies for safety evaluation of nanomaterials. Part VI. Characterization of nanoscale particles for toxicological evaluation. Toxicol Sci 90:296–303. doi: 10.1093/toxsci/kfj09910.1093/toxsci/kfj099 ↗
50. Rahman Q, Norwood J, Hatch G (1997) Evidence that exposure of particulate air pollutants to human and rat alveolar macrophages leads to differential oxidative response. Biochem Biophys Res Commun 240:669–672. doi: 10.1016/j.bbr.2011.03.03110.1006/bbrc.1997.7373 ↗
51. Rahman Q, Lohani M, Dopp E, Pemsel H, Jonas L, Weiss DG, Schiffmann D (2002) Evidence that ultrafine titanium dioxide induces micronuclei and apoptosis in Syrian hamsters embryo fibroblasts. Environ Health Perspect 110:797–800. doi: 10.1289/ehp.0211079710.1289/ehp.02110797 ↗
52. Reeves JF, Davies SJ, Dodd NJF, 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. doi: 10.1016/j.mrfmmm.2007.12.01010.1016/j.mrfmmm.2007.12.010 ↗
53. Renwick LC, Donaldson K, Clouter A (2001) Impairment of alveolar macrophage phagocytosis by ultrafine particles. Toxicol Appl Pharmacol 172:119–127. doi: 10.1006/taap.2001.912810.1006/taap.2001.9128 ↗
54. Reyes-Coronado D, Rodríguez-Gattorno G, Espinosa-Pesqueira ME, Cab C, de Coss R, Oskam G (2008) Phase-pure TiO2 nanoparticles: anatase, brookite and rutile. Nanotechnology 19:145605–145615. doi: 10.1088/0957-4484/19/14/14560510.1088/0957-4484/19/14/145605 ↗
55. Roh JY, Park YK, Park K, Choi J (2010) Ecotoxicological investigation of CeO2 and TiO2 nanoparticles on the soil nematode Caenorhabditis elegans using gene expression, growth, fertility, and survival as endpoints. Environ Toxicol Pharmacol 29:167–172. doi: 10.1016/j.etap.2009.12.00310.1016/j.etap.2009.12.003 ↗
56. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
57. Sayes CM, Gobin AM, Ausman KD, Mendez J, West JL, Colvin VL (2005) Nano-C60 cytotoxicity is due to lipid peroxidation. Biomaterials 26:7587–7595. doi: 10.1186/1477-3155-4-1410.1016/j.biomaterials.2005.05.027 ↗
58. Singh S, Shi T, Duffin R, Albrecht C, van Berlo D, Hohr D, Fubini B, Martra G, Fenoglio I, Borm PJA, Schins PF (2007) Endocytosis, oxidative stress and IL-8 expression in human lung epithelial cells upon treatment with fine and ultrafine TiO2: role of the specific surface area and of surface methylation of the particles. Toxicol Appl Pharm 222:141–151. doi: 10.1016/j.taap.2007.05.00110.1016/j.taap.2007.05.001 ↗
59. Smith CJ, Shaw BJ, Handy RD (2007) Toxicity of single walled carbon nanotubes to rainbow trout, (Oncorhynchus mykiss): respiratory toxicity, organ pathologies, and other physiological effects. Aquat Toxicol 82:94–109. doi: 10.1016/j.aquatox.2007.02.00310.1016/j.aquatox.2007.02.003 ↗
60. Van Hoecke K, De Schamphelaere KAC, Van der Meeren P, Lucas S, Janssen CR (2008) Ecotoxicity of silica nanoparticles to the green alga Pseudokirchneriella subcapitata: importance of surface area. Environ Toxicol Chem 27:1948–1957. doi: 10.1897/07-634.110.1897/07-634.1 ↗
61. Wang JJ, Sanderson BJS, Wang H (2007) Cyto- and genotoxicity of ultrafine TiO2 particles in cultured human lymphoblastoid cells. Mutat Res 628:99–106. doi: 10.1016/j.mrgentox.2006.12.00310.1016/j.mrgentox.2006.12.003 ↗
62. Warheit DB, Webb TR, Reed KL, Frerichs S, Sayes CM (2007) Pulmonary toxicity study in rats with three forms of ultrafine-TiO2 particles: differential responses related to surface properties. Toxicology 230:90–104. doi: 10.1016/j.tox.2006.11.00210.1016/j.tox.2006.11.002 ↗
63. Xia T, Korge P, Weiss JN, Li N, Venkatesen MI, Sioutas C, Nel A (2004) Quinones and aromatic chemicals compounds in particulate matter induce mitochondrial dysfunction: implications for ultrafine particle toxicity. Environ Health Perspect 112:1347–1358. doi: 10.1289/ehp.716710.1289/ehp.7167 ↗
64. Yin H, Too HP, Chow GM (2005) The effects of particle size and surface coating on the cytotoxicity of nickel ferrite. Biomaterials 26:5818–5826. doi: 10.1016/j.biomaterials.2005.02.03610.1016/j.biomaterials.2005.02.036 ↗
65. Zhu S, Oberdorster E, Haasch ML (2006) Toxicity of an engineered nanoparticle (fullerene, C60) in two aquatic species, Daphnia and fathead minnow. Mar Environ Res 62(Supplement 1):S5–S9. doi: 10.1016/j.marenvres.2006.04.05910.1016/j.marenvres.2006.04.059 ↗
66. Zhu X, Zhu L, Duan Z, Qi R, Li Y, Lang Y (2008a) Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to Zebrafish (Danio rerio) early developmental stage. J Environ Sci Health A 43:278–284. doi: 10.1080/1093452070179277910.1080/10934520701792779 ↗
67. Zhu X, Zhu L, Lang Y, Chen Y (2008b) Oxidative stress and growth inhibition in the freshwater fish Carassius auratus induced by chronic exposure to sublethal fullerene aggregates. Environ Toxicol Chem 27:1979–1985. doi: 10.1897/07-573.110.1897/07-573.1 ↗
68. Zhu X, Zhu L, Chen Y, Tian S (2009) Acute toxicities of six manufactured nanomaterial suspensions to Daphnia magna. J Nanopart Res 11:67–75. doi: 10.1007/s11051-008-9426-810.1007/s11051-008-9426-8 ↗
69. Zhu X, Zhou J, Cai Z (2011) The toxicity and oxidative stress of TiO2 nanoparticles in marine abalone. (Haliotis diversicolor supertexta). Mar Pollut Bull 63:334–338. doi: 10.1016/j.marpolbul.2011.03.00610.1016/j.marpolbul.2011.03.006 ↗