Reproductive Toxicity Induction in Nematodes Exposed to Environmental Toxicants or Stresses

  • Dayong Wang


Reproductive organs are important secondary targeted organs for environmental toxicants in nematodes. We here mainly introduced and discussed the potential reproductive toxicity of environmental toxicants or stresses on brood size, generation time, egg-laying, gonad development, and gametogenesis in hermaphrodite nematodes. Moreover, we further introduced and discussed the potential reproductive toxicity of environmental toxicants or stresses on male nematodes, such as toxicity in increasing the rate of male formation, toxicity on male structures, sex-specific response to environmental exposure, and effects from the mating behavior.


Reproductive toxicity Environmental exposure Caenorhabditis elegans 


  1. 1.
    Wang D-Y (2018) Nanotoxicology in Caenorhabditis elegans. Springer, SingaporeCrossRefGoogle Scholar
  2. 2.
    Wang D-Y (2018) Molecular Toxicology in Caenorhabditis elegans. Springer, SingaporeCrossRefGoogle Scholar
  3. 3.
    Ding X-C, Rui Q, Wang D-Y (2018) Functional disruption in epidermal barrier enhances toxicity and accumulation of graphene oxide. Ecotoxicol Environ Saf 163:456–464CrossRefGoogle Scholar
  4. 4.
    Xiao G-S, Zhao L, Huang Q, Du H-H, Guo D-Q, Xia M-X, Li G-M, Chen Z-X, Wang D-Y (2018) Biosafety assessment of water samples from Wanzhou watershed of Yangtze Three Gorges Reservoir in the quiet season in Caenorhabditis elegans. Sci Rep 8:14102CrossRefGoogle Scholar
  5. 5.
    Wang D-Y, Yu Y-L, Li Y-X, Wang Y, Wang D-Y (2014) Dopamine receptors antagonistically regulate behavioral choice between conflicting alternatives in C. elegans. PLoS ONE 9:e115985CrossRefGoogle Scholar
  6. 6.
    Li Y-X, Wang Y, Hu Y-O, Zhong J-X, Wang D-Y (2011) Modulation of the assay system for the sensory integration of 2 sensory stimuli that inhibit each other in nematode Caenorhabditis elegans. Neurosci Bull 27:69–82CrossRefGoogle Scholar
  7. 7.
    Ruan Q-L, Qiao Y, Zhao Y-L, Xu Y, Wang M, Duan J-A, Wang DY. (2016) Beneficial effects of Glycyrrhizae radix extract in preventing oxidative damage and extending the lifespan of Caenorhabditis elegans. J Ethnopharmacol 177: 101–110CrossRefGoogle Scholar
  8. 8.
    Yu Y-L, Zhi L-T, Wu Q-L, Jing L-N, Wang D-Y (2018) NPR-9 regulates innate immune response in Caenorhabditis elegans by antagonizing activity of AIB interneurons. Cell Mol Immunol 15:27–37CrossRefGoogle Scholar
  9. 9.
    Zhi L-T, Yu Y-L, Jiang Z-X, Wang D-Y (2017) mir-355 functions as an important link between p38 MAPK signaling and insulin signaling in the regulation of innate immunity. Sci Rep 7:14560CrossRefGoogle Scholar
  10. 10.
    Yu Y-L, Zhi L-T, Guan X-M, Wang D-Y, Wang D-Y (2016) FLP-4 neuropeptide and its receptor in a neuronal circuit regulate preference choice through functions of ASH-2 trithorax complex in Caenorhabditis elegans. Sci Rep 6:21485CrossRefGoogle Scholar
  11. 11.
    Guo Y-L, Yang Y-C, Wang D-Y (2009) Induction of reproductive deficits in nematode Caenorhabditis elegans exposed to metals at different developmental stages. Reprod Toxicol 28:90–95CrossRefGoogle Scholar
  12. 12.
    Smith MA Jr, Zhang Y, Polli JR, Wu H, Zhang B, Xiao P, Farwell MA, Pan X (2013) Impacts of chronic low-level nicotine exposure on Caenorhabditis elegans reproduction: identification of novel gene targets. Reprod Toxicol 40:69–75CrossRefGoogle Scholar
  13. 13.
    Wu Q-L, He K-W, Liu P-D, Li Y-X, Wang D-Y (2011) Association of oxidative stress with the formation of reproductive toxicity from mercury exposure on hermaphrodite nematode Caenorhabditis elegans. Environ Toxicol Pharmacol 32:175–184CrossRefGoogle Scholar
  14. 14.
    Teshiba E, Miyahara K, Takeya H (2016) Glucose-induced abnormal egg-laying rate in Caenorhabditis elegans. Biosci Biotechnol Biochem 80:1436–1439CrossRefGoogle Scholar
  15. 15.
    Kumar S, Aninat C, Michaux G, Morel F (2010) Anticancer drug 5-fluorouracil induces reproductive and developmental defects in Caenorhabditis elegans. Reprod Toxicol 29:415–420CrossRefGoogle Scholar
  16. 16.
    Estevez AO, Mueller CL, Morgan KL, Szewczyk NJ, Teece L, Miranda-Vizuete A, Estevez M (2012) Selenium induces cholinergic motor neuron degeneration in Caenorhabditis elegans. Neurotoxicology 33:1021–1032CrossRefGoogle Scholar
  17. 17.
    Allard P, Colaiácovo MP (2010) Bisphenol A impairs the double-strand break repair machinery in the germline and causes chromosome abnormalities. Proc Natl Acad Sci U S A 107:20405–20410CrossRefGoogle Scholar
  18. 18.
    Webster CM, Deline ML, Watts JL (2013) Stress response pathways protect germ cells from omega-6 polyunsaturated fatty acid-mediated toxicity in Caenorhabditis elegans. Dev Biol 373:14–25CrossRefGoogle Scholar
  19. 19.
    Zhao Y-L, Wu Q-L, Li Y-P, Wang D-Y (2013) Translocation, transfer, and in vivo safety evaluation of engineered nanomaterials in the non-mammalian alternative toxicity assay model of nematode Caenorhabditis elegans. RSC Adv 3:5741–5757CrossRefGoogle Scholar
  20. 20.
    Shao H-M, Han Z-Y, Krasteva N, Wang D-Y (2018) Identification of signaling cascade in the insulin signaling pathway in response to nanopolystyrene particles. Nanotoxicology.
  21. 21.
    Wang Q-Q, Zhao S-Q, Zhao Y-L, Rui Q, Wang D-Y (2014) Toxicity and translocation of graphene oxide in Arabidopsis plants under stress conditions. RSC Adv 4:60891–60901CrossRefGoogle Scholar
  22. 22.
    Polli JR, Zhang Y, Pan X (2014) Dispersed crude oil amplifies germ cell apoptosis in Caenorhabditis elegans, followed a CEP-1-dependent pathway. Arch Toxicol 88:543–551PubMedGoogle Scholar
  23. 23.
    Yang H-C, Chen T-L, Wu Y-H, Cheng K-P, Lin Y-H, Cheng M-L, Ho H-Y, Lo SJ, DT-Y C (2013) Glucose 6-phosphate dehydrogenase deficiency enhances germ cell apoptosis and causes defective embryogenesis in Caenorhabditis elegans. Cell Death Dis 4:e616CrossRefGoogle Scholar
  24. 24.
    Allard P, Kleinstreuer NC, Knudsen TB, Colaiácovo MP (2013) A C. elegans screening platform for the rapid assessment of chemical disruption of germline function. Environ Health Perspect 121:717–724CrossRefGoogle Scholar
  25. 25.
    O’Donnell B, Huo L, Polli JR, Qiu L, Collier DN, Zhang B, Pan X (2017) ZnO nanoparticles enhanced germ cell apoptosis in Caenorhabditis elegans, in comparison with ZnCl2. Toxicol Sci 156:336–343PubMedGoogle Scholar
  26. 26.
    Wang S, Zhao Y, Wu L, Tang M, Su C, Hei TK, Yu Z (2007) Induction of germline cell cycle arrest and apoptosis by sodium arsenite in Caenorhabditis elegans. Chem Res Toxicol 20:181–186CrossRefGoogle Scholar
  27. 27.
    Zhao Y-L, Wu Q-L, Wang D-T (2016) An epigenetic signal encoded protection mechanism is activated by graphene oxide to inhibit its induced reproductive toxicity in Caenorhabditis elegans. Biomaterials 79:15–24CrossRefGoogle Scholar
  28. 28.
    Wang S, Geng Z, Wang Y, Tong Z, Yu H (2012) Essential roles of p53 and MAPK cascades in microcystin-LR-induced germline apoptosis in Caenorhabditis elegans. Environ Sci Technol 46:3442–3448CrossRefGoogle Scholar
  29. 29.
    Wang S, Wu L, Wang Y, Luo X, Lu Y (2009) Copper-induced germline apoptosis in Caenorhabditis elegans: the independent roles of DNA damage response signaling and the dependent roles of MAPK cascades. Chem-Biol Int 180:151–157CrossRefGoogle Scholar
  30. 30.
    Pei B, Wang S, Guo X, Wang J, Yang G, Hang H, Wu L (2008) Arsenite-induced germline apoptosis through a MAPK-dependent, p53-independent pathway in Caenorhabditis elegans. Chem Res Toxicol 21:1530–1535CrossRefGoogle Scholar
  31. 31.
    Wang Y, Wang S, Luo X, Yang Y, Jian F, Wang X, Xie L (2014) The roles of DNA damage-dependent signals and MAPK cascades in tributyltin-induced germline apoptosis in Caenorhabditis elegans. Chemosphere 108:231–238CrossRefGoogle Scholar
  32. 32.
    Wang S, Tang M, Pei B, Xiao X, Wang J, Hang H, Wu L (2008) Cadmium-induced germline apoptosis in Caenorhabditis elegans: the roles of HUS1, p53, and MAPK signaling pathways. Toxicol Sci 102:345–351CrossRefGoogle Scholar
  33. 33.
    Cheng Z, Tian H, Chu H, Wu J, Li Y, Wang Y (2014) The effect of tributyltin chloride on Caenorhabditis elegans germline is mediated by a conserved DNA damage checkpoint pathway. Toxicol Lett 225:413–421CrossRefGoogle Scholar
  34. 34.
    Du H, Wang M, Dai H, Hong W, Wang M, Wang J, Weng N, Nie Y, Xu A (2015) Endosulfan isomers and sulfate metabolite induced reproductive toxicity in Caenorhabditis elegans involves genotoxic response genes. Environ Sci Technol 49:2460–2468CrossRefGoogle Scholar
  35. 35.
    VanDuyn N, Settivari R, Wong G, Nass R (2010) SKN-1/Nrf2 inhibits dopamine neuron degeneration in a Caenorhabditis elegans model of methylmercury toxicity. Toxicol Sci 118:613–624CrossRefGoogle Scholar
  36. 36.
    Chen Y, Shu L, Qiu Z, Lee DY, Settle SJ, Que Hee S, Telesca D, Yang X, Allard P (2016) Exposure to the BPA substitute Bisphenol S causes unique alterations of germline function. PLoS Genet 12:e1006223CrossRefGoogle Scholar
  37. 37.
    Guo X, Bian P, Liang J, Wang Y, Li L, Wang J, Yuan H, Chen S, Xu A, Wu L (2014) Synergistic effects induced by a low dose of diesel particulate extract and ultraviolet-A in Caenorhabditis elegans: DNA damage-triggered germ cell apoptosis. Chem Res Toxicol 27:990–1001CrossRefGoogle Scholar
  38. 38.
    You X, Xi J, Cao Y, Zhang J, Luan Y (2017) 4-Bromodiphenyl ether induces germ cell apoptosis by induction of ROS and DNA damage in Caenorhabditis elegans. Toxicol Sci 157:510–518CrossRefGoogle Scholar
  39. 39.
    Ruan Q-L, Ju J-J, Li Y-H, Li X-B, Liu R, Liang G-Y, Zhang J, Pu Y-P, Wang D-Y, Yin L-H (2012) Chlorpyrifos exposure reduces reproductive capacity owing to a damaging effect on gametogenesis in the nematode Caenorhabditis elegans. J Appl Toxicol 32:527–535CrossRefGoogle Scholar
  40. 40.
    Li Y, Zhang M, Chen P, Liu R, Liang G, Yin L, Pu Y (2015) Effects of microcystin-LR exposure on spermiogenesis in nematode Caenorhabditis elegans. Int J Mol Sci 16:22927–22937CrossRefGoogle Scholar
  41. 41.
    Kong L, Gao X, Zhu J, Zhang T, Xue Y, Tang M (2017) Reproductive toxicity induced by nickel nanoparticles in Caenorhabditis elegans. Environ Toxicol 32:1530–1538CrossRefGoogle Scholar
  42. 42.
    Yin J-C, Liu R, Jian Z-H, Yang D, Pu Y-P, Yin L-H, Wang D-Y (2018) Di (2-ethylhexyl) phthalate-induced reproductive toxicity involved in DNA damage-dependent oocyte apoptosis and oxidative stress in Caenorhabditis elegans. Ecotoxicol Environ Saf 163:298–306CrossRefGoogle Scholar
  43. 43.
    Liu P-D, He K-W, Li Y-X, Wu Q-L, Yang P, Wang D-Y (2012) Exposure to mercury causes formation of male-specific structural deficits by inducing oxidative damage in nematodes. Ecotoxicol Environ Saf 79:90–100CrossRefGoogle Scholar
  44. 44.
    Ruszkiewicz JA, de Macedo GT, Miranda-Vizuete A, Bowman AB, Bornhorst J, Schwerdtle5 T, Soares FAA, Aschner M (2018) Sex-specific response of Caenorhabditis elegans to methylmercury toxicity. Neurotox Res. CrossRefGoogle Scholar
  45. 45.
    Shi C, Murphy CT (2014) Mating induces shrinking and death in Caenorhabditis mothers. Science 343:536–540CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Dayong Wang
    • 1
  1. 1.School of MedicineSoutheast UniversityNanjingChina

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