Skip to main content

Omics in Zebrafish Teratogenesis

  • Protocol
  • First Online:
Teratogenicity Testing

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1797))

Abstract

The genome revolution represents a complete change on our view of biological systems. The quantitative determination of changes in all major molecular components of the living cells, the “omics” approach, opened whole new fields for all health sciences. Genomics, transcriptomics, proteomics, metabolomics, and others, together with appropriate prediction and modeling tools, will mark the future of developmental toxicity assessment both for wildlife and humans. This is especially true for disciplines, like teratology, which rely on studies in model organisms, as studies at lower levels of organization are difficult to implement. Rodents and frogs have been the favorite models for studying human reproductive and developmental disorders for decades. Recently, the study of the development of zebrafish embryos (ZE) is becoming a major alternative tool to adult animal testing. ZE intrinsic characteristics makes this model a unique system to analyze in vivo developmental alterations that only can be studied applying in toto approaches. Moreover, under actual legislations, ZE is considered as a replacement model (and therefore, excluded from animal welfare regulations) during the first 5 days after fertilization. Here we review the most important components of the zebrafish toolbox available for analyzing early stages of embryotoxic events that could eventually lead to teratogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Sogorb MA, Pamies D, de Lapuente J et al (2014) An integrated approach for detecting embryotoxicity and developmental toxicity of environmental contaminants using in vitro alternative methods. Toxicol Lett 230(2):356–367. https://doi.org/10.1016/j.toxlet.2014.01.037

    Article  PubMed  CAS  Google Scholar 

  2. Love DR, Pichler FB, Dodd A et al (2004) Technology for high-throughput screens: the present and future using zebrafish. Curr Opin Biotechnol 15(6):564–571. https://doi.org/10.1016/j.copbio.2004.09.004

    Article  PubMed  CAS  Google Scholar 

  3. Goldsmith P (2004) Zebrafish as a pharmacological tool: the how, why and when. Curr Opin Pharmacol 4(5):504–512. https://doi.org/10.1016/j.coph.2004.04.005

    Article  PubMed  CAS  Google Scholar 

  4. Zon LI, Peterson RT (2005) In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 4(1):35–44. https://doi.org/10.1038/nrd1606

    Article  PubMed  CAS  Google Scholar 

  5. McGrath P, Li CQ (2008) Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov Today 13(9-10):394–401. https://doi.org/10.1016/j.drudis.2008.03.002

    Article  PubMed  CAS  Google Scholar 

  6. Berghmans S, Butler P, Goldsmith P et al (2008) Zebrafish based assays for the assessment of cardiac, visual and gut function--potential safety screens for early drug discovery. J Pharmacol Toxicol Methods 58(1):59–68. https://doi.org/10.1016/j.vascn.2008.05.130

    Article  PubMed  CAS  Google Scholar 

  7. Russell WMS, Burch RL (1959) The principles of humane experimental techniques. Methuen, London

    Google Scholar 

  8. EFSA (2005) Opinion of the Scientific Panel on Animal Health and Welfare on a request from the Commission related to the aspects of the biology and welfare of animals used for experimental and other scientific purposes (EFSA-Q-2004-105). EFSA J 292:1–46

    Google Scholar 

  9. Heijne WH, Kienhuis AS, van Ommen B et al (2005) Systems toxicology: applications of toxicogenomics, transcriptomics, proteomics and metabolomics in toxicology. Expert Rev Proteomics 2(5):767–780. https://doi.org/10.1586/14789450.2.5.767

    Article  PubMed  CAS  Google Scholar 

  10. Ouedraogo M, Baudoux T, Stevigny C et al (2012) Review of current and “omics” methods for assessing the toxicity (genotoxicity, teratogenicity and nephrotoxicity) of herbal medicines and mushrooms. J Ethnopharmacol 140(3):492–512. https://doi.org/10.1016/j.jep.2012.01.059

    Article  PubMed  CAS  Google Scholar 

  11. Aardema MJ, MacGregor JT (2002) Toxicology and genetic toxicology in the new era of “toxicogenomics”: impact of “-omics” technologies. Mutat Res 499(1):13–25

    Article  PubMed  CAS  Google Scholar 

  12. Merrick BA, Bruno ME (2004) Genomic and proteomic profiling for biomarkers and signature profiles of toxicity. Curr Opin Mol Ther 6(6):600–607

    PubMed  CAS  Google Scholar 

  13. Miranda RC, Pietrzykowski AZ, Tang Y et al (2010) MicroRNAs: master regulators of ethanol abuse and toxicity? Alcohol Clin Exp Res 34(4):575–587. https://doi.org/10.1111/j.1530-0277.2009.01126.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Colleoni S, Galli C, Gaspar JA et al (2011) Development of a neural teratogenicity test based on human embryonic stem cells: response to retinoic acid exposure. Toxicol Sci 124(2):370–377. https://doi.org/10.1093/toxsci/kfr245

    Article  PubMed  CAS  Google Scholar 

  15. Hashimoto-Torii K, Kawasawa YI, Kuhn A, Rakic P (2011) Combined transcriptome analysis of fetal human and mouse cerebral cortex exposed to alcohol. Proc Natl Acad Sci U S A 108(10):4212–4217. https://doi.org/10.1073/pnas.1100903108

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lossie AC, Muir WM, Lo CL et al (2014) Implications of genomic signatures in the differential vulnerability to fetal alcohol exposure in C57BL/6 and DBA/2 mice. Front Genet 5:173. https://doi.org/10.3389/fgene.2014.00173

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Shinde V, Perumal Srinivasan S, Henry M et al (2016) Comparison of a teratogenic transcriptome-based predictive test based on human embryonic versus inducible pluripotent stem cells. Stem Cell Res Ther 7(1):190. https://doi.org/10.1186/s13287-016-0449-2

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Yang L, Kemadjou JR, Zinsmeister C et al (2007) Transcriptional profiling reveals barcode-like toxicogenomic responses in the zebrafish embryo. Genome Biol 8(10):R227. https://doi.org/10.1186/gb-2007-8-10-r227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Yang L, Ho NY, Alshut R et al (2009) Zebrafish embryos as models for embryotoxic and teratological effects of chemicals. Reprod Toxicol 28(2):245–253. https://doi.org/10.1016/j.reprotox.2009.04.013

    Article  PubMed  CAS  Google Scholar 

  20. Hermsen SAB, Pronk TE, van den Brandhof EJ et al (2013) Transcriptomic analysis in the developing zebrafish embryo after compound exposure: individual gene expression and pathway regulation. Toxicol Appl Pharmacol 272(1):161–171. https://doi.org/10.1016/j.taap.2013.05.037

    Article  PubMed  CAS  Google Scholar 

  21. van der Laan JW, Chapin RE, Haenen B et al (2012) Testing strategies for embryo-fetal toxicity of human pharmaceuticals. Animal models vs. in vitro approaches: a workshop report. Regul Toxicol Pharmacol 63(1):115–123. https://doi.org/10.1016/j.yrtph.2012.03.009

    Article  PubMed  CAS  Google Scholar 

  22. Fang X, Corrales J, Thornton C et al (2015) Transcriptomic changes in zebrafish embryos and larvae following benzo a pyrene exposure. Toxicol Sci 146(2):395–411. https://doi.org/10.1093/toxsci/kfv105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Mesquita SR, van Drooge BL, Oliveira E et al (2015) Differential embryotoxicity of the organic pollutants in rural and urban air particles. Environ Pollut 206:535–542. https://doi.org/10.1016/j.envpol.2015.08.008

    Article  PubMed  CAS  Google Scholar 

  24. Olivares A, van Drooge BL, Casado M et al (2013) Developmental effects of aerosols and coal burning particles in zebrafish embryos. Environ Pollut 178:72–79. https://doi.org/10.1016/j.envpol.2013.02.026

    Article  PubMed  CAS  Google Scholar 

  25. Raldua D, Thienpont B, Babin PJ (2012) Zebrafish eleutheroembryos as an alternative system for screening chemicals disrupting the mammalian thyroid gland morphogenesis and function. Reprod Toxicol 33(2):188–197. https://doi.org/10.1016/j.reprotox.2011.09.001

    Article  PubMed  CAS  Google Scholar 

  26. Pelayo S, Oliveira E, Thienpont B et al (2012) Triiodothyronine-induced changes in the zebrafish transcriptome during the eleutheroembryonic stage: implications for bisphenol A developmental toxicity. Aquat Toxicol 110:114–122. https://doi.org/10.1016/j.aquatox.2011.12.016

    Article  PubMed  CAS  Google Scholar 

  27. Hanson MA, Gluckman PD (2007) The role of epigenetics in developmental plasticity and developmental induction of risk of adult disease. Am J Phys Anthropol: Suppl 44, 125

    Google Scholar 

  28. Gluckman PD, Hanson MA, Low FM (2011) The role of developmental plasticity and epigenetics in human health. Birth Defects Res C Embryo Today 93(1):12–18. https://doi.org/10.1002/bdrc.20198

    Article  PubMed  CAS  Google Scholar 

  29. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(Suppl):245–254. https://doi.org/10.1038/ng1089

    Article  CAS  PubMed  Google Scholar 

  30. Westeberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278. https://doi.org/10.1146/annurev.es.20.110189.001341

    Article  Google Scholar 

  31. Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319(5871):1827–1830. https://doi.org/10.1126/science.1153069

    Article  PubMed  CAS  Google Scholar 

  32. Hashida S, Kitamura K, Mikami T, Kishima Y (2003) Temperature shift coordinately changes the activity and the methylation state of transposon Tam3 in Antirrhinum majus. Plant Physiol 132(3):1207–1216. https://doi.org/10.1104/pp.102.017533

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Oberlander TF, Weinberg J, Papsdorf M et al (2008) Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3(2):97–106

    Article  PubMed  Google Scholar 

  34. Ambros V (2004) The functions of animal microRNAs. Nature 431(7006):350–355. https://doi.org/10.1038/nature02871

    Article  PubMed  CAS  Google Scholar 

  35. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297. https://doi.org/10.1016/s0092-8674(04)00045-5

    Article  PubMed  CAS  Google Scholar 

  36. Griffiths-Jones S (2004) The microRNA Registry. Nucleic Acids Res 32:D109–D111. https://doi.org/10.1093/nar/gkh023

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Pappalardo-Carter DL, Balaraman S, Sathyan P et al (2013) Suppression and epigenetic regulation of MiR-9 contributes to ethanol teratology: evidence from zebrafish and murine fetal neural stem cell models. Alcohol Clin Exp Res 37(10):1657–1667. https://doi.org/10.1111/acer.12139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Wang L-L, Zhang Z, Li Q et al (2009) Ethanol exposure induces differential microRNA and target gene expression and teratogenic effects which can be suppressed by folic acid supplementation. Hum Reprod 24(3):562–579. https://doi.org/10.1093/humrep/den439

    Article  PubMed  CAS  Google Scholar 

  39. Williams TD, Mirbahai L, Chipman JK (2014) The toxicological application of transcriptomics and epigenomics in zebrafish and other teleosts. Brief Funct Genomics 13(2):157–171. https://doi.org/10.1093/bfgp/elt053

    Article  PubMed  Google Scholar 

  40. Sanchez BC, Ralston-Hooper K, Sepulveda MS (2011) Review of recent proteomic applications in aquatic toxicology. Environ Toxicol Chem 30(2):274–282. https://doi.org/10.1002/etc.402

    Article  PubMed  CAS  Google Scholar 

  41. Groebe K, Hayess K, Klemm-Manns M et al (2010) Protein biomarkers for in vitro testing of embryotoxicity. J Proteome Res 9(11):5727–5738. https://doi.org/10.1021/pr100514e

    Article  PubMed  CAS  Google Scholar 

  42. Hanisch K, Kuster E, Altenburger R, Gundel U (2010) Proteomic signatures of the zebrafish (Danio rerio) embryo: sensitivity and specificity in toxicity assessment of chemicals. Int J Proteomics 2010:630134. https://doi.org/10.1155/2010/630134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Baral R, Wetie AGN, Darie CC, Wallace KN (2014) Mass spectrometry for proteomics-based investigation using the zebrafish vertebrate model system. In: Woods AG, Darie CC (eds) Advancements of mass spectrometry in biomedical research, Advances in experimental medicine and biology, vol 806. Springer, Berlin. https://doi.org/10.1007/978-3-319-06068-2_15

    Chapter  Google Scholar 

  44. Bantscheff M, Lemeer S, Savitski MM, Kuster B (2012) Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Anal Bioanal Chem 404(4):939–965. https://doi.org/10.1007/s00216-012-6203-4

    Article  PubMed  CAS  Google Scholar 

  45. Meganathan K, Jagtap S, Wagh V et al (2012) Identification of thalidomide-specific transcriptomics and proteomics signatures during differentiation of human embryonic stem cells. PLoS One 7(8):e44228. https://doi.org/10.1371/journal.pone.0044228

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Chen H, Boontheung P, Loo RR et al (2008) Proteomic analysis to characterize differential mouse strain sensitivity to cadmium-induced forelimb teratogenesis. Birt Defects Res A Clin Mol Teratol 82(4):187–199. https://doi.org/10.1002/bdra.20444

    Article  CAS  Google Scholar 

  47. Chen Y, Lin PX, Hsieh CL et al (2014) The proteomic and genomic teratogenicity elicited by valproic acid is preventable with resveratrol and alpha-tocopherol. PLoS One 9(12):e116534. https://doi.org/10.1371/journal.pone.0116534

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Chen H, Song Q, Diao X, Zhou H (2016) Proteomic and metabolomic analysis on the toxicological effects of Benzo[a]pyrene in pearl oyster Pinctada martensii. Aquat Toxicol 175:81–89. https://doi.org/10.1016/j.aquatox.2016.03.012

    Article  PubMed  CAS  Google Scholar 

  49. Bale A, Szabo D, Nath R, Vulimiri S (2012) Potential use of 'omics data in a mode-of-action analysis of neurobehavioral toxicity of methylmercury. Neurotoxicol Teratol 34(3):379–379. https://doi.org/10.1016/j.ntt.2012.05.035

    Article  CAS  Google Scholar 

  50. Datta S, Turner D, Singh R et al (2008) Fetal alcohol syndrome (FAS) in C57BL/6 mice detected through proteomics screening of the amniotic fluid. Birt Defects Res A Clin Mol Teratol 82(4):177–186. https://doi.org/10.1002/bdra.20440

    Article  CAS  Google Scholar 

  51. Verma N, Pink M, Rettenmeier AW, Schmitz-Spanke S (2012) Review on proteomic analyses of benzo a pyrene toxicity. Proteomics 12(11):1731–1755. https://doi.org/10.1002/pmic.201100466

    Article  PubMed  CAS  Google Scholar 

  52. Canales L, Chen J, Birtles T et al (2010) Altered liver proteome profiles in a mouse model of “developmental” cigarette smoke exposure. Birth Defects Res A Clin Mol Teratol 88(5):355–355

    Google Scholar 

  53. Shi X, Yeung LWY, Lam PKS et al (2009) Protein profiles in Zebrafish (Danio rerio) embryos exposed to perfluorooctane sulfonate. Toxicol Sci 110(2):334–340. https://doi.org/10.1093/toxsci/kfp111

    Article  PubMed  CAS  Google Scholar 

  54. Olavarria J, Machin A, Possessky S et al (2014) Targeted proteomic analysis associated with an in vitro zebrafish developmental toxicology assay using LC-MS/MS. Birth Defects Res A Clin Mol Teratol 100(5):429–429

    Google Scholar 

  55. Zheng L, Yu JL, Shi HH et al (2015) Quantitative toxicoproteomic analysis of zebrafish embryos exposed to a retinoid X receptor antagonist UVI3003. J Appl Toxicol 35(9):1049–1057. https://doi.org/10.1002/jat.3099

    Article  PubMed  CAS  Google Scholar 

  56. van Ravenzwaay B, Cunha GC-P, Leibold E et al (2007) The use of metabolomics for the discovery of new biomarkers of effect. Toxicol Lett 172(1-2):21–28. https://doi.org/10.1016/j.toxlet.2007.05.021

    Article  PubMed  CAS  Google Scholar 

  57. Lindon JC, Nicholson JK (2008) Analytical technologies for metabonomics and metabolomics, and multi-omic information recovery. Trends Anal Chem 27(3):194–204. https://doi.org/10.1016/j.trac.2007.08.009

    Article  CAS  Google Scholar 

  58. Smith AM, Palmer JA, West PR et al (2013) A metabolomics-based assay to rapidly predict mammalian developmental toxicity using human pluripotent stem cells (hPSCs). Birth Defects Res A Clin Mol Teratol 97(5):291–291

    Google Scholar 

  59. Benskin JP, Ikonomou MG, Liu J et al (2014) Distinctive metabolite profiles in in-migrating sockeye salmon suggest sex-linked endocrine perturbation. Environ Sci Technol 48(19):11670–11678. https://doi.org/10.1021/es503266x

    Article  PubMed  CAS  Google Scholar 

  60. Zheng X, Su M, Pei L et al (2011) Metabolic signature of pregnant women with neural tube defects in offspring. J Proteome Res 10(10):4845–4854. https://doi.org/10.1021/pr200666d

    Article  PubMed  CAS  Google Scholar 

  61. Rochester JR (2013) Bisphenol A and human health: a review of the literature. Reprod Toxicol 42:132–155. https://doi.org/10.1016/j.reprotox.2013.08.008

    Article  PubMed  CAS  Google Scholar 

  62. Andersson T, Forlin L (1985) Spectral properties of substrate cytochrome P-450 interaction and catalytic activity of xenobiotic metabolizing enzymes in isolated rainbow-trout liver cells. Biochem Pharmacol 34(9):1407–1413

    Article  PubMed  CAS  Google Scholar 

  63. Busquet F, Nagel R, von Landenberg F et al (2008) Development of a new screening assay to identify proteratogenic substances using zebrafish danio rerio embryo combined with an exogenous mammalian metabolic activation system (mDarT). Toxicol Sci 104(1):177–188. https://doi.org/10.1093/toxsci/kfn065

    Article  PubMed  CAS  Google Scholar 

  64. German JB, Gillies LA, Smilowitz JT et al (2007) Lipidomics and lipid profiling in metabolomics. Curr Opin Lipidol 18(1):66–71

    PubMed  CAS  Google Scholar 

  65. Jordao R, Casas J, Fabrias G et al (2015) Obesogens beyond vertebrates: lipid perturbation by tributyltin in the crustacean daphnia magna. Environ Health Perspect 123(8):813–819. https://doi.org/10.1289/ehp.1409163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Zhou XA, Zhou J, Tian HC, Yuan YJ (2010) Dynamic lipidomic insights into the adaptive responses of saccharomyces cerevisiae to the repeated vacuum fermentation. OMICS 14(5):563–574. https://doi.org/10.1089/omi.2010.0016

    Article  PubMed  CAS  Google Scholar 

  67. Bonet ML, Ribot J, Palou A (2012) Lipid metabolism in mammalian tissues and its control by retinoic acid. Biochim Biophys Acta 1821(1):177–189. https://doi.org/10.1016/j.bbalip.2011.06.001

    Article  PubMed  CAS  Google Scholar 

  68. Raldua D, Andre M, Babin PJ (2008) Clofibrate and gemfibrozil induce an embryonic malabsorption syndrome in zebrafish. Toxicol Appl Pharmacol 228(3):301–314. https://doi.org/10.1016/j.taap.2007.11.016

    Article  PubMed  CAS  Google Scholar 

  69. Santos EM, Ball JS, Williams TD et al (2010) Identifying health impacts of exposure to copper using transcriptomics and metabolomics in a fish model. Environ Sci Technol 44(2):820–826. https://doi.org/10.1021/es902558k

    Article  PubMed  CAS  Google Scholar 

  70. Huang SSY, Benskin JP, Veldhoen N et al (2017) A multi-omic approach to elucidate low-dose effects of xenobiotics in zebrafish (Danio rerio) larvae. Aquat Toxicol 182:102–112. https://doi.org/10.1016/j.aquatox.2016.11.016

    Article  PubMed  CAS  Google Scholar 

  71. Williams TD, Wu HF, Santos EM et al (2009) Hepatic transcriptomic and metabolomic responses in the stickleback (gasterosteus aculeatus) exposed to environmentally relevant concentrations of dibenzanthracene. Environ Sci Technol 43(16):6341–6348. https://doi.org/10.1021/es9008689

    Article  PubMed  CAS  Google Scholar 

  72. Ji C, Wu H, Wei L et al (2013) Proteomic and metabolomic analysis reveal gender-specific responses of mussel Mytilus galloprovincialis to 2,2',4,4'-tetrabromodiphenyl ether (BDE 47). Aquat Toxicol 140-141:449–457. https://doi.org/10.1016/j.aquatox.2013.07.009

    Article  PubMed  CAS  Google Scholar 

  73. Katsiadaki I, Williams TD, Ball JS et al (2010) Hepatic transcriptomic and metabolomic responses in the Stickleback (Gasterosteus aculeatus) exposed to ethinyl-estradiol. Aquat Toxicol 97(3):174–187

    Article  PubMed  CAS  Google Scholar 

  74. Soanes KH, Achenbach JC, Burton IW et al (2011) Molecular characterization of zebrafish embryogenesis via dna microarrays and multiplatform time course metabolomics studies. J Proteome Res 10(11):5102–5117. https://doi.org/10.1021/Pr2005549

    Article  PubMed  CAS  Google Scholar 

  75. Deal S, Wambaugh J, Judson R et al (2016) Development of a quantitative morphological assessment of toxicant-treated zebrafish larvae using brightfield imaging and high-content analysis. J Appl Toxicol 36(9):1214–1222. https://doi.org/10.1002/jat.3290

    Article  PubMed  CAS  Google Scholar 

  76. Oliveira E, Casado M, Raldua D et al (2013) Retinoic acid receptors’ expression and function during zebrafish early development. J Steroid Biochem Mol Biol 138:143–151. https://doi.org/10.1016/j.jsbmb.2013.03.011

    Article  PubMed  CAS  Google Scholar 

  77. Dombkowski AA, Thibodeau BJ, Starcevic SL, Novak RF (2004) Gene-specific dye bias in microarray reference designs. FEBS Lett 560(1):120–124. https://doi.org/10.1016/S0014-5793(04)00083-3

    Article  PubMed  CAS  Google Scholar 

  78. Jaumot J, Navarro A, Faria M et al (2015) qRT-PCR evaluation of the transcriptional response of zebra mussel to heavy metals. BMC Genomics 16:354. https://doi.org/10.1186/s12864-015-1567-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Ortiz-Villanueva E, Benavente F, Pina B et al (2017) Knowledge integration strategies for untargeted metabolomics based on MCR-ALS analysis of CE-MS and LC-MS data. Anal Chim Acta 978:10–23. https://doi.org/10.1016/j.aca.2017.04.049

    Article  PubMed  CAS  Google Scholar 

  80. Puig-Castellvi F, Alfonso I, Pina B, Tauler R (2016) H-1 NMR metabolomic study of auxotrophic starvation in yeast using multivariate curve resolution-alternating least squares for pathway analysis. Sci Rep 6:30982. https://doi.org/10.1038/srep30982

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Jaumot J, Pina B, Tauler R (2010) Application of multivariate curve resolution to the analysis of yeast genome-wide screens. Chemom Intel Lab Syst 104(1):53–64. https://doi.org/10.1016/j.chemolab.2010.04.004

    Article  CAS  Google Scholar 

  82. Ucar D, Neuhaus I, Ross-MacDonald P et al (2007) Construction of a reference gene association network from multiple profiling data: application to data analysis. Bioinformatics 23(20):2716–2724. https://doi.org/10.1093/bioinformatics/btm423

    Article  PubMed  CAS  Google Scholar 

  83. WHO (2002) World health report. World Health Organization, Geneva

    Google Scholar 

  84. Nielsen G, Gee D (2012) The impacts of endocrine disrupters on wildlife, people and their environments. The Weybridge+15 (1996-2011) report. EEA Technical Report, vol 2.

    Google Scholar 

  85. Wang A, Padula A, Sirota M, Woodruff TJ (2016) Environmental influences on reproductive health: the importance of chemical exposures. Fertil Steril 106(4):905–929. https://doi.org/10.1016/j.fertnstert.2016.07.1076

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Spanish Ministry of Economy and Competitiveness (CTM2014-51985), the NATO Science for Peace and Security Programme (SFP-984777), and the Generalitat de Catalunya (grant 2014SGR642).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Benjamin Piña .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Piña, B., Navarro, L., Barata, C., Raldúa, D., Martínez, R., Casado, M. (2018). Omics in Zebrafish Teratogenesis. In: Félix, L. (eds) Teratogenicity Testing. Methods in Molecular Biology, vol 1797. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7883-0_23

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-7883-0_23

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-7882-3

  • Online ISBN: 978-1-4939-7883-0

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics