Assessing variation in the potential susceptibility of fish to pharmaceuticals, considering evolutionary differences in their physiology and ecology

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1656, 2014, Pages

  Brown, A R ^a,b   Gunnarsson, L ^c   Kristiansson, E ^d   Tyler, C R ^b  

^a ASTRAZENECA   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Drug target; Orthologue; Physiology; Population ecology; Species; Susceptibility

Indexed keywords

ADAPTATION; DRUG; FISH; HORMONE; LIFE HISTORY TRAIT; LIFE TABLE; LIGAND; POPULATION GROWTH; RISK ASSESSMENT;

DRUG; WATER POLLUTANT;

AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; ECOSYSTEM; EVOLUTION; FISH; GENETICS; PHYLOGENY; PHYSIOLOGY; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; TOXICITY; WATER POLLUTANT;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; ECOSYSTEM; FISHES; MODELS, BIOLOGICAL; PHARMACEUTICAL PREPARATIONS; PHYLOGENY; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; WATER POLLUTANTS, CHEMICAL;

EID: 85003055518     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0576     Document Type: Article

References (71)

1. Knox C et al. 2011 DrugBank 3. 0: a comprehensive resource for 'Omics' research on drugs. Nucleic Acids Res. 39(Suppl. 1), D1035-D1041. (doi: 10. 1093/nar/gkq1126).
2. National Institutes of Health 2014 Therapeutic drug levels: medline plus. See http://www. nlm. nih. gov/medlineplus/ency/article/003430. htm (accessed January 2014).
3. Gunnarsson L, Jauhiainen A, Kristiansson E, Nerman O, Larsson DG. 2008 Evolutionary conservation of human drug targets in organisms used for environmental risk assessments. Environ. Sci. Technol. 42, 5807-5813. (doi: 10. 1021/es8005173).
4. Kostich MS, Lazorchak JM. 2008 Risks to aquatic organisms posed by human pharmaceutical use. Sci. Total Environ. 389, 329-339. (doi: 10. 1016/j. scitotenv. 2007. 09. 008).
5. Lalone CA et al. 2013 Molecular target sequence similarity as a basis for species extrapolation to assess the ecological risk of chemicals with known modes of action. Aquat. Toxicol. 144-145, 141-154. (doi: 10. 1016/j. aquatox. 2013. 09. 004).
6. McRobb FM, Sahagún V, Kufareva I, Abagyan R. 2014 In silico analysis of the conservation of human toxicity and endocrine disruption targets in aquatic species. Environ. Sci. Technol. 48, 1964-1972. (doi: 10. 1021/es404568a).
7. Daughton CG, Ternes TA. 1999 Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ. Health Perspect. 107(Suppl. 6), 907-938. (doi: 10. 1289/ehp. 99107s6907).
8. Snyder SA. 2008 Occurrence, treatment, and toxicological relevance of EDCs and pharmaceuticals in water. Ozone-Sci. Eng. 30, 65-69. (doi: 10. 1080/01919510701799278).
9. Barber LB, Keefe SH, Brown GK, Furlong ET, Gray JL, Kolpin DW, Meyer MT, Sandstrom MW, Zaugg SD. 2013 Persistence and potential effects of complex organic contaminant mixtures in wastewaterimpacted streams. Environ. Sci. Technol. 7, 2177-2188. (doi: 10. 1021/es303720g).
10. Oaks JL. 2004 Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 427, 630-633. (doi: 10. 1038/nature02317).
11. Cuthbert RJ et al. 2014 Avian scavengers and the threat from veterinary pharmaceuticals. Phil. Trans. R. Soc. B 369, 20130574. (doi: 10. 1098/rstb. 2013. 0574).
12. Jobling S et al. 2002 Wild intersex roach (Rutilus rutilus) have reduced fertility. Biol. Reprod. 67, 515-524. (doi: 10. 1095/biolreprod67. 2. 515).
13. Palace VP, Evans RE, Wautier KG, Mills KH, Blanchfield PJ, Park BJ, Baron CL, Kidd KA. 2009 Interspecies differences in biochemical, histopathological, and population responses in four wild fish species exposed to ethynylestradiol added to a whole lake. Can. J. Fish. Aquat. Sci. 66, 1920-1935. (doi: 10. 1139/F09-125).
14. Harris CA et al. 2010 The consequences of feminization in breeding groups of wild fish. Environ. Health Perspect. 119, 306-311. (doi: 10. 1289/ehp. 1002555).
15. Kidd KA, Paterson MJ, Rennie MD, Podemski CL, Findlay DL, Blanchfield PJ, Liber K. 2014 Direct and indirect responses of a freshwater food web to a potent synthetic oestrogen. Phil. Trans. R. Soc. B 369, 20130578. (doi: 10. 1098/rstb. 2013. 0578).
16. Caldwell DJ, Mastrocco F, Margiotta-Casaluci L, Brooks BW. 2014 An integrated approach for prioritizing pharmaceuticals found in the environment for risk assessment, monitoring and advanced research. Chemosphere (doi: 10. 1016/j. chemosphere. 2014. 01. 021).
17. Schreiber R, Gündel U, Franz S, Küster A, Rechenberg B, Altenburger R. 2011 Using the fish plasma model for comparative hazard identification for pharmaceuticals in the environment by extrapolation from human therapeutic data. Regul. Toxicol. Pharmacol. 61, 261-275. (doi: 10. 1016/j. yrtph. 2011. 08. 006).
18. Roos V, Gunnarsson L, Fick J, Larsson DG, Rudén C. 2012 Prioritising pharmaceuticals for environmental risk assessment: towards adequate and feasible first-tier selection. Sci. Tot. Environ. 421-422, 102-110. (doi: 10. 1016/j. scitotenv. 2012. 01. 039).
19. Huggett DB, Cook JC, Ericson JF, Williams RT. 2003 A theoretical model for utilizing mammalian pharmacology and safety data to prioritize potential impacts of human pharmaceuticals to fish. Hum. Ecol. Risk Assess. 9, 1789-1799. (doi: 10. 1080/714044797).
20. Nelson JS. 2006 Fishes of the world, 4th edn, p. 624. Hoboken, NJ: John Wiley and Sons.
21. Broughton RE, Betancur-R R, Li C, Arratia G, Ortí G. 2013 Multi-locus phylogenetic analysis reveals the pattern and tempo of bony fish evolution. PLoS Curr. 5. (doi: 10. 1371/currents. tol. 2ca8041495ffa fd0c92756e75247483e).
22. Van Straalen NM. 1994 Biodiversity of ecotoxicological responses in animals. Neth. J. Zool. 44, 112-129. (doi: 10. 1163/156854294X00097).
23. Du B et al. 2014 Bioaccumulation and trophic dilution of human pharmaceuticals across trophic positions of an effluent-dependent wadeable stream. Phil. Trans. R. Soc. B 369, 20140058. (doi: 10. 1098/rstb. 2014. 0058).
24. Brodin T, Piovano S, Fick J, Klaminder J, Heynen M, Jonsson M. 2014 Ecological effects of pharmaceuticals in aquatic systems-impacts through behavioural alterations. Phil. Trans. R. Soc. B 369, 20130580. (doi: 10. 1098/rstb. 2013. 0580).
25. European Medicines Agency 2006 Guideline on the environmental risk assessment of medicinal product for human use. London, UK: EMEA/CHMP/SWP4447/00.
26. Rand-Weaver M, Margiotta-Casaluci L, Patel A, Panter GH, Owen SF, Sumpter JP. 2013 The readacross hypothesis and environmental risk assessment of pharmaceuticals. Environ. Sci. Technol. 47, 11 384-11 395. (doi: 10. 1021/es402065a).
27. Fitzsimmons PN, Fernandez JD, Hoffman AD, Butterworth BC, Nichols JW. 2001 Branchial elimination of superhydrophobic organic compounds by rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 55, 23-34. (doi: 10. 1016/S0166-445X(01)00174-6).
28. Hutchinson TH, Madden JC, Naidoo V, Walker CH. 2014 Comparative metabolism as a key driver of wildlife species sensitivity to human and veterinary pharmaceuticals. Phil. Trans. R. Soc. B 369, 20130583. (doi: 10. 1098/rstb. 2013. 0583).
29. Corcoran J, Lange A, Cumming RI, Owen SF, Ball JS, Tyler CR, Winter MJ. 2014 Bioavailability of the imidazole antifungal agent clotrimazole and its effects on key PXR-regulated genes in the common carp (Cyprinus carpio). Aquat. Toxicol. 152C, 57-65. (doi: 10. 1016/j. aquatox. 2014. 03. 016).
30. Miguel-Queralt S, Hammond GL. 2008 Sex hormone-binding globulin in fish gills is a portal for sex steroids breached by xenobiotics. Endocrinology 149, 4269-4275. (doi: 10. 1210/en. 2008-0384).
31. Shimada T, Yamazaki H, Mimura M, Inui Y, Guengerich FP. 1994 Inter-individual variations in human liver cytochrome P-450 enzymes involved in the oxidation of drugs, carcinogens, and toxic chemicals: studies with liver microsomes of 30 Japanese and 30 Caucasians. J. Pharm. Exp. Ther. 270, 414-423.
32. Connors KA, Du B, Fitzsimmons PN, Hoffman AD, Chambliss CK, Nichols JW, Brooks BW. 2013 Comparative pharmaceutical metabolism by rainbow trout (Oncorhynchus mykiss) liver S9 fractions. Environ. Toxicol. Chem. 32, 1810-1818. (doi: 10. 1002/etc. 2240).
33. Milnes MR et al. 2008 Activation of steroid and xenobiotic receptor (SXR, NR1I2) and its orthologs in laboratory, toxicologic, and genome model species. Environ. Health Perspect. 116, 880-885. (doi: 10. 1289/ehp. 10853).
34. Flicek P et al. 2013 Ensembl. Nucleic Acids Res. 41, D48-D55. (doi: 10. 1093/nar/gks1236).
35. Kristensen DM, Wolf YI, Mushegian AR, Koonin EV. 2011 Computational methods for gene orthology inference. Brief Bioinform. 12, 379-391. (doi: 10. 1093/bib/bbr030).
36. Meyer A, Van de Peer Y. 2005 From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27, 937-945. (doi: 10. 1002/bies. 20293).
37. Miyagawa S et al. 2014 Differing species responsiveness of estrogenic contaminants in fish is conferred by the ligand binding domain of the estrogen receptor. Environ. Sci. Technol. 48, 5254-5263. (doi: 10. 1021/es5002659).
38. Spromberg JA, Birge WJ. 2005 Population survivorship index for fish and amphibians: application to criterion development and risk assessment. Environ. Toxicol. Chem. 24, 1541-1547. (doi: 10. 1897/04-159. 1).
39. De Lange HJ, Lahr J, Van der Pol JJ, Wessels Y, Faber JH. 2009 Ecological vulnerability in wildlife: an expert judgment and multicriteria analysis tool using ecological traits to assess relative impact of pollutants. Environ. Toxicol. Chem. 28, 2233-2240. (doi: 10. 1897/08-626. 1).
40. Van den Brink PJ, Baird DJ, Baveco HJM, Focks A. 2013 The use of traits-based approaches and eco(toxico)logical models to advance the ecological risk assessment framework for chemicals. Integr. Environ. Assess. Manag. 9, e47-e57. (doi: 10. 1002/ieam. 1443).
41. Brown AR, Riddle AM, Cunningham NL, Kedwards TJ, Shillabeer N, Hutchinson TH. 2003 Predicting the effects of endocrine disruptors on fish populations. Hum. Ecol. Risk Assess. 9, 761-788. (doi: 10. 1080/713609966).
42. Schwindt AR, Winkelman DL, Keteles K, Murphy M, Vajda AM. 2014 An environmental oestrogen disrupts fish population dynamics through direct and transgenerational effects on survival and fecundity. J. Appl. Ecol. (doi: 10. 1111/1365-2664. 12237).
43. Länge R, Hutchinson TH, Croudace CP, Siegmund F, Schweinfurth H, Hampe P, Panter GH, Sumpter JP. 2001 Effects of the synthetic estrogen 17 a-ethinyloestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 20, 1216-1227. (doi: 10. 1002/etc. 5620200610).
44. Schäfers C, Teigeler M, Wenzel A, Maack G, Fenske M, Segner H. 2007 Concentration-and timedependent effects of the synthetic estrogen, 17 a-ethinyloestradiol, on reproductive capabilities of the zebrafish, Danio rerio. J. Toxicol. Environ. Health A. 70, 768-779. (doi: 10. 1080/1528739070 1236470).
45. Zha J, Sun L, Zhou Y, Spear PA, Ma M, Wang Z. 2008 Assessment of 17 a-ethinylestradiol effects and underlying mechanisms in a continuous, multigeneration exposure of the Chinese rare minnow (Gobiocypris rarus). Toxicol. Appl. Pharmacol. 226, 298-308. (doi: 10. 1016/j. taap. 2007. 10. 006).
46. Vilella AJ, Severin J, Ureta-Vidal A, Durbin R, Heng L, Bimey E. 2009 EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 19, 327-335. (doi: 10. 1101/gr. 073585. 107).
47. UniProt 2013 Consortium, Update on activities at the Universal Protein Research (UniProt) in 2013. Nucleic Acids Res. 41, D43-D47. (doi: 10. 1093/nar/gks1068).
48. National Centre for Biotechnology Information. 2014 Taxonomy database. See www. ncbi. nln. nih. gov/taxonomy (accessed February 2014).
49. Marchler-Bauer A et al. 2013 CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res. 41, D348-D352. (doi: 10. 1093/nar/gks1243).
50. Kufareva I, Ilatovskiy AV, Abagyan R. 2012 Pocketome: an encyclopedia of small-molecule binding sites in 4D. Nucleic Acids Res. 40, D535-D540. (doi: 10. 1093/nar/gkr825).
51. Froese R, Pauly D (eds). 2013 FishBase. See http://www. fishbase. org (accessed December 2013).
52. Xie Z, Frimpong EA, Lee S. 2013 FishTraits version 2: integrating ecological, biogeographic and bibliographic information. In Proc. 13th ACM/IEEE-CS joint Conference on Digital Libraries, pp. 447-448. New York, NY: ACM. See http://www. fishtraits. info/search/attr/(accessed December 2013).
53. Ågerstrand M, Breitholtz M, Rudén C. 2011 Comparison of four different methods for reliability evaluation of ecotoxicity data: a case study of nonstandard test data used in environmental risk assessments of pharmaceutical substances. Environ. Sci. Eur. 23, 17. (doi: 10. 1186/2190-4715-23-17).
54. Nash JP, Kime DE, Van der Ven LT, Wester PW, Brion F, Maack G, Stahlschmidt-Allner P, Tyler CR. 2004 Longterm exposure to environmental concentrations of the pharmaceutical ethynyloestradiol causes reproductive failure in fish. Environ. Health Perspect. 112, 1725-1733. (doi: 10. 1289/ehp. 7209).
55. Soares J et al. 2009 Disruption of zebrafish (Danio rerio) embryonic development after full life-cycle parental exposure to low levels of ethinyloestradiol. Aquat. Toxicol. 95, 330. (doi: 10. 1016/j. aquatox. 2009. 07. 021).
56. Scholz S, Gutzeit HO. 2000 17 a-Ethinyloestradiol affects reproduction, sexual differentiation and aromatase gene expression of the medaka (Oryzias latipes). Aquat. Toxicol. 50, 363-373. (doi: 10. 1016/S0166-445X(00)00090-4).
57. Balch GC, Mackenzie CA, Metcalf CD. 2004 Alterations to gonadal development and reproductive success in Japanese medaka (Oryzias latipes) exposed to 17aethinyloestradiol. Environ. Toxicol. Chem. 23, 782-791. (doi: 10. 1897/02-539).
58. Hood GM. 2010 PopTools version 3. 2. 5. See http://www. poptools. org.
59. Miller DH, Ankley GT. 2004 Modeling impacts on populations: fathead minnow (Pimephales promelas) exposure to the endocrine disruptor 17 b-trenbolone as a case study. Ecotoxicol. Environ. Saf. 59, 1-9. (doi: 10. 1016/j. ecoenv. 2004. 05. 005).
60. Meng Y, Lin B-L, Tominga M, Nakanishi J. 2006 Simulations of the population-level effects of 4 nonyl-phenol on wild Japanese medaka (Oryzias latipes). Ecol. Model. 197, 350-360. (doi: 10. 1016/j. ecolmodel. 2006. 03. 022).
61. Hazlerigg CRE, Tyler CR, Lorenzen K, Wheeler JR, Thorbek P. 2014 Population relevance of toxicant mediated changes in sex ratio in fish: an assessment using an individual-based zebrafish (Danio rerio) model. Ecol. Model. (doi: 10. 1016/j. ecolmodel. 2013. 12. 016).
62. Caswell H. 1996 Analysis of life table response experiments II. Alternative parameterizations for size-and stage-structured models. Ecol. Model. 88, 73-82. (doi: 10. 1016/0304-3800(95)00070-4).
63. Gharib WH, Robinson-Rechavi M. 2011 When orthologs diverge between human and mouse. Brief Bioinform. 12, 436-441. (doi: 10. 1093/bib/bbr031).
64. Bridgham JT, Carroll SM, Thornton JW. 2006 Evolution of hormone-receptor complexity by molecular exploitation. Science 312, 97-101. (doi: 10. 1126/science. 1123348).
65. Bryan MB, Scott AP, Li W. 2008 Sex steroids and their receptors in lampreys. Steroids 73, 1-12. (doi: 10. 1016/j. steroids. 2007. 08. 011).
66. Lee O, Takesono A, Tada M, Tyler CR, Kudoh T. 2012 Biosensor zebrafish provide new insights into potential health effects of environmental estrogens. Environ. Health Perspect. 120, 990-996. (doi: 10. 1289/ehp. 1104433).
67. Segner H, Casanova-Nakayama A, Kase R, Tyler CR. 2013 Impact of environmental estrogens on fish considering the diversity of estrogen signaling. Gen. Comp. Endocrinol. 191, 190-201. (doi: 10. 1016/j. ygcen. 2013. 05. 015).
68. Matthews JB, Clemons JH, Zacharewski TR. 2001 Reciprocal mutagenesis between human (L349, M528) and rainbow trout (M317, I496) estrogen receptor residues demonstrates their importance in ligand binding and gene expression at different temperatures. Mol. Cell. Endocrinol. 183, 127-139. (doi: 10. 1016/S0303-7207(01)00586-X).
69. Schreurs RHMM, Quaedackers ME, Seinen W, van der Burg B. 2002 Transcriptional activation of estrogen receptor ERa and ERb by polycyclic musks is cell type dependent. Toxicol. Appl. Pharmacol. 15, 183-192. (doi: 10. 1006/taap. 2002. 9458).
70. Mims MC, Olden JD, Shattuck ZR, Poff NL. 2010 Life history trait diversity of native freshwater fishes in North America. Ecol. Freshw. Fish 19, 390-400. (doi: 10. 1111/j. 1600-0633. 2010. 00422. x).
71. Larsen MG, Hansen KB, Henriksen PG, Baatrup E. 2008 Male zebrafish (Danio rerio) courtship behaviour resists the feminising effects of 17 a-ethinyloestradiol, morphological sexual characteristics do not. Aquat. Toxicol. 87, 234-244. (doi: 10. 1016/j. aquatox. 2008. 02. 003).