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The Specific Cases of Pahs and Metal Oxide Nanoparticles

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The Specific Cases of Pahs and Metal Oxide Nanoparticles Cell Biology in Environmental Toxicology Group DEPARTMENT OF ZOOLOGY AND ANIMAL CELL BIOLOGY ZOOLOGIA ETA ANIMALIA ZELULEN BIOLOGIA SAILA DEPARTAMENTO DE ZOOLOGÍA Y BIOLOGÍA CELULAR ANIMAL Cellular and molecular responses of zebrafish to legacy and emerging pollutants: the specific cases of PAHs and metal oxide nanoparticles International Ph. D. Thesis submitted by UNAI VICARIO PARÉS for the degree of Philosophiae Doctor December 2015 “A la família. Per mantenir-me dempeus quan no volia caminar” ACKNOWLEDGMENTS Funding This study was funded by: - European Commission (7th Framework Program) through the NanoReTox project “The reactivity and toxicity of engineered nanoparticles: risks to the environment and human health” (CP-FP 214478-2, 2008-­‐2012). - The Spanish Ministry of Science and Technology by means of the CANCERMAR project “Mecanismos celulares y moleculares de carcinogénesis química en organismos acuáticos: aplicaciones para la evaluación de la calidad del medio marino” (CTM2006-06192) and NANOCANCER project “Determinación del potencial genotóxico y carcinogénico de las nanopartículas metálicas mediante la utilización de métodos alternativos in vitro e in vivo con peces cebra e invertebrados“ (CTM2009- 13477). -The Spanish Ministry of Science and Innovation through a mobility grant to obtain the European PhD degree. - The Basque Government through a grant to consolidated Research Groups (GIC07/26-IT-393-07 and IT810-13). - The University of the Basque Country by means of a predoctoral grant and a grant to the Unit of Formation and Research “Protection of Ecosystem Health” (UFI11/37). Acknowledgments I wish to thank all the people and institutions that helped me to carry out this Ph.D. research. Without their support none of this would have been possible. - Dr. Amaia Orbea supervisor of this Ph.D. thesis, for giving me the opportunity to perform this research work and for her support and guidance during these years. - Dr. Dries Knapen and Dr. Lucia Vergauwen (University of Antwerp) for their teaching and help in the mircoarray analysis interpretation. - Consolidated research group “Cell Biology in Environmental Toxicology” of the Department of Zoology and Cell Biology of the University of the Basque Country, for contributing either directly or indirectly to carrying out this work. I really appreciate the pleasure of working in a team. Index I. Introduction ................................................................. 1 A. Legacy and emerging pollutants .................................. 5 A.1. Legacy organic pollutants. A specific case: PAHs........... 6 A.2. Emerging pollutants. A specific case: metal oxide nanoparticles....................................................................... 12 B. Effects of PAHs to fish ..................................................... 17 B.1. Bioaccumulation of PAHs.............................................. 18 B.2. Transcriptomic effects of PAHs..................................... 18 B.3. Enzymatic effects of PAHs............................................. 19 B.4. Genetic effects of PAHs................................................. 20 B.5. Immunological effects of PAHs...................................... 20 B.6. Cellular effects of PAHs................................................. 21 B.7. Histopathological effects of PAHs................................. 21 B.8. Developmental effects of PAHs..................................... 22 C. Effects of metals and metal oxide NPs to fish .......... 24 C.1. Effects of metals to fish................................................. 24 C.1.1. Bioaccumulation of metals .............................................. 25 C.1.2. Transcriptomic and enzymatic effects of metals ................... 25 C.1.3. Genetic effects of metals ................................................. 26 C.1.4. Cellular effects of metals ................................................. 27 C.1.5. Histopathological effects of metals .................................... 27 C.1.6. Developmental effects of metals ...................................... 28 C.2. Effects of metal oxide NPs to fish.................................. 28 C.2.1. Bioaccumulation ............................................................ 30 C.2.2. Transcriptomic and enzymatic effects of metal oxide NPs ...... 30 C.2.3. Genetic effects of metal oxide NPs ..................................... 31 C.2.4. Immunological effects of metal oxide NPs ........................... 31 C.2.5. Histopathological effects of metal oxide NPs ........................ 32 C.2.6. Developmental effects of metal oxide NPs ........................... 32 I Index D. The zebrafish model ......................................................... 47 D.1. Characteristics and natural distribution......................... 47 D.2. Reproduction and development.................................... 48 D.3. Advantages of zebrafish as model organism.................. 51 D.4. Zebrafish in ecotoxicology.............................................. 53 II. State of the art, Hypothesis and Objectives ........................................................................... 81 III. Results and Discussion ...................................... 87 Chapter I: Cellular and molecular effects of waterborne exposure of adult zebrafish to carcinogenic PAHs.................... 89 Chapter II: Effects of waterborne exposure to carcinogenic PAHs on adult zebrafish hepatic transcriptome......................... 121 Chapter III: Long-term transcriptional and histopathological effects in zebrafish exposed to B( a)P and/or DMBA during embryogenesis.................................................................. 157 Chapter IV: Comparative toxicity of metal oxide nanoparticles (CuO, ZnO and TiO 2) to developing zebrafish embryos....................................................................... 183 Chapter V: Cellular and molecular responses of adult zebrafish after exposure to CuO nanoparticles or ionic copper.................................................................................. 213 IV. General Discussion ............................................... 245 V. Conclusions and Thesis ...................................... 265 II I. INTRODUCTION ABBREVIATIONS Most relevant abbreviations 7,12-dimethylbenz(a)anthracene, DMBA Adverse outcome pathway, AOP Aldo-keto reductase, AKR Aryl hydrocarbon receptor, AHR Aryl hydrocarbon receptor repressor, AHRR Aryl hydrocarbon receptor nuclear translocator, ARNT American society for testing and materials, ASTM Benzo(a)pyrene, B(a)P Catalase, CAT Days post-fertilization, dpf Emerging pollutants, EPs Environmental risk assessment, ERA Epoxide hydrolase, EH Estrogen receptor, ER Glutathione, GSH Glutathione S-transferase, GST Hours post-fertilization, hpf International agency for research on cancer, IARC International organization for standardization, ISO Metallothionein, MT Mode of action, MOA 3 INTRODUCTION Molecular initiating event, MIE Molecular weight, MW NADP(H)-quinone oxidoreductase 1, NQO1 Nanomaterial, NM Nanoparticle, NP Organization of economic co-operation and development, OECD Polycyclic aromatic hydrocarbon, PAH Registration, evaluation, authorization and restriction of chemicals, REACH Reactive oxygen species, ROS Sulfotransferase, SULT Superoxide dismutase, SOD UDP-glucuronosyltransferase, UGT Xenobiotic response element, XRE 4 A. LEGACY AND EMERGING POLLUTANTS A. LEGACY AND EMERGING POLLUTANTS Historically chemical wastes generated through industrial processes have been disposed of through flagrant release into the environment (Leblanc 2004). Consequently, at the present time there are approximately 100,000 chemicals in the environment, with an additional 500-1,000 added each year (Laws 2012). Many of those anthropogenic residues have found their ultimate fate in water bodies allowing their dilution and efficient transport away from the site of generation (Leblanc 2004). Potential adverse effects of the introduction of such anthropogenic chemicals into the environment were viewed as insignificant relative to the benefits bestowed by such practices (Leblanc 2004). The potential damaging capacity of all those substances is not always known. Thus, we have historically assumed a risk to the human and environmental health that is continuously threatened by the presence of both the pre-existing and the newly generated pollutants (Sauvé and Desrosiers 2014). Since the early sixties, mankind has become aware of the potential long-term adverse effects of these chemicals in general and their potential risks for aquatic and terrestrial ecosystems in particular (Van der Oost et al. 2003). Luckily, awakening of the general public to the hazards of chemicals have led public organizations and governments to regulate and limit the release of chemicals to the environment (Leblanc 2004). The European regulation (EC) No. 1907/2006 (EU 2006) concerning the Registration, Evaluation, Authorization and Restriction of Chemicals (REACH) together with the establishment of an European Chemicals Agency (ECHA), supposed a turning point in the protection of human and environmental health. In order to implement effective and sustainable regulations, extensive knowledge on the effects of chemicals to the environment and the human health is essential (Deblonde et al. 2011). Environmental toxicology aims to assess the adverse effects of environmental chemicals through different scientific disciplines. The ultimate goal of these assessments is elucidating the adverse effects of chemicals that are
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