Advertisement

Molecular Basis for Oxidative Stress Induced by Environmental Toxicants in Nematodes

  • Dayong Wang
Chapter

Abstract

Oxidative stress plays an important role in the toxicity induction of environmental toxicants or stresses in nematodes. Usually, this is the first cellular mechanism needed to be clarified for the toxicity formation of certain environmental toxicants or stresses. We here systematically introduced both the molecular machinery for the activation of oxidative stress and the response signals with the functions to defend against the oxidative stress in nematodes. Moreover, we explained the molecular basis for the induction of oxidative stress in nematodes exposed to environmental toxicants.

Keywords

Molecular basis Oxidative stress Environmental toxicant Caenorhabditis elegans 

References

  1. 1.
    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 79:90–100PubMedCrossRefGoogle Scholar
  2. 2.
    Nouara A, Wu Q-L, Li Y-X, Tang M, Wang H-F, Zhao Y-L, Wang D-Y (2013) Carboxylic acid functionalization prevents the translocation of multi-walled carbon nanotubes at predicted environmental relevant concentrations into targeted organs of nematode Caenorhabditis elegans. Nanoscale 5:6088–6096PubMedCrossRefGoogle Scholar
  3. 3.
    Kayser EB, Morgan PG, Hoppel CL, Sedensky MM (2001) Mitochondrial expression and function of GAS-1 in Caenorhabditis elegans. J Biol Chem 276:20551–20558PubMedCrossRefGoogle Scholar
  4. 4.
    Kayser E, Sedensky MM, Morgan PG (2004) The effects of complex I function and oxidative damage on lifespan and anesthetic sensitivity in Caenorhabditis elegans. Mech Ageing Dev 125:455–464PubMedCrossRefGoogle Scholar
  5. 5.
    Dingley S, Polyak E, Lightfoot R, Ostrovsky J, Rao M, Greco T, Ischiropoulos H, Falk MJ (2010) Mitochondrial respiratory chain dysfunction variably increases oxidant stress in Caenorhabditis elegans. Mitochondrion 10:125–136PubMedCrossRefGoogle Scholar
  6. 6.
    Yang W, Hekimi S (2010) A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biol 8:e1000556PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Ishii N, Fujii M, Hartman PS, Tsuda M, Yasuda K, Senoo-Matsuda N, Yanase S, Ayusawa D, Suzuki K (1998) A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 394:694–697PubMedCrossRefGoogle Scholar
  8. 8.
    Senoo-Matsuda N, Yasuda K, Tsuda M, Ohkubo T, Yoshimura S, Nakazawa H, Hartman PS, Ishii N (2001) A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans. J Biol Chem 276:41553–41558PubMedCrossRefGoogle Scholar
  9. 9.
    Feng J, Bussiere F, Hekimi S (2001) Mitochondrial electron transport is a key determinant of life span in Caenorhabditis elegans. Dev Cell 1:633–644PubMedCrossRefGoogle Scholar
  10. 10.
    Dues DJ, Schaar CE, Johnson BK, Bowman MJ, Winn ME, Senchuk MM, Van Raamsdonk JM (2017) Uncoupling of oxidative stress resistance and lifespan in long-lived isp-1 mitochondrial mutants in Caenorhabditis elegans. Free Radic Biol Med 108:362–373PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Miyadera H, Amino H, Hiraishi A, Taka H, Murayama K, Miyoshi H, Sakamoto K, Ishii N, Hekimi S, Kita K (2001) Altered quinone biosynthesis in the long-lived clk-1 mutants of Caenorhabditis elegans. J Biol Chem 276:7713–7716PubMedCrossRefGoogle Scholar
  12. 12.
    Schaar CE, Dues DJ, Spielbauer KK, Machiela E, Cooper JF, Senchuk M, Hekimi S, Van Raamsdonk JM (2015) Mitochondrial and cytoplasmic ROS have opposing effects on lifespan. PLoS Genet 11:e1004972PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Monaghan RM, Barnes RG, Fisher K, Andreou T, Rooney N, Poulin GB, Whitmarsh AJ (2015) A nuclear role for the respiratory enzyme CLK-1 in regulating mitochondrial stress responses and longevity. Nat Cell Biol 17:782–792PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Anderson GL (1982) Superoxide dismutase activity in dauer larvae of C. elegans (Nematoda: Rhabditidae). Can J Zool 60:288–291CrossRefGoogle Scholar
  15. 15.
    Yanase S, Onodera A, Tedesco P, Johnson TE, Ishii N (2009) SOD-1 deletions in Caenorhabditis elegans alter the localization of intracellular reactive oxygen species and show molecular compensation. J Gerontol A Biol Sci Med Sci 64:530–539PubMedCrossRefGoogle Scholar
  16. 16.
    Van Raamsdonk JM, Hekimi S (2009) Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans. PLoS Genet 5:e1000361PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Doonan RT, McElwee JJ, Matthijssens F, Walker GA, Houthoofd KB, Back P, Matscheski A, Vanfleteren JR, Gems DH (2008) Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev 22:3236–3241PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Petriv OI, Rachubinski RA (2004) Lack of peroxisomal catalase causes a progeric phenotype in Caenorhabditis elegans. J Biol Chem 279:19996–20001PubMedCrossRefGoogle Scholar
  19. 19.
    Larsen PL (1993) Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci U S A 90:8905–8909PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Honda Y, Honda S (1999) The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J 13:1385–1393PubMedCrossRefGoogle Scholar
  21. 21.
    Kondo M, Senoo-Matsuda N, Yanase S, Ishii T, Hartman PS, Ishii N (2005) Effect of oxidative stress on translocation of DAF-16 in oxygen-sensitive mutants, mev-1 and gas-1 of Caenorhabditis elegans. Mech Ageing Dev 126:637–641PubMedCrossRefGoogle Scholar
  22. 22.
    Chavez V, Mohri-Shiomi A, Maadani A, Veqa LA, Garsin DA (2007) Oxidative stress enzymes are required for DAF-16-mediated immunity due to generation of reactive oxygen species by Caenorhabditis elegans. Genetics 176:1567–1577PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, Korswagen HC (2005) Functional interaction between β-catenin and FOXO in oxidative stress signaling. Science 308:1181–1184PubMedCrossRefGoogle Scholar
  24. 24.
    Khare S, Gomez T, Clarke SG (2009) Defective responses to oxidative stress in protein L-isoaspartyl repair-deficient Caenorhabditis elegans. Mech Ageing Dev 130:670–680PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    An JH, Blackwell TK (2003) SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev 17:1882–1893PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Li H, Liu X, Wang D, Su L, Zhao T, Li Z, Lin C, Zhang Y, Huang B, Lu J, Li X (2017) O-GlcNAcylation of SKN-1 modulates the lifespan and oxidative stress resistance in Caenorhabditis elegans. Sci Rep 7:43601PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Staab TA, Egrafov O, Knowles JA, Sieburth D (2014) Regulation of synaptic nlg-1/neuroligin abundance by the skn-1/Nrf stress response pathway protects against oxidative stress. PLoS Genet 10:e1004100PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Tullet JMA, Green JW, Au C, benedetto A, Thompson MA, Clark E, Gillat AF, Young A, Schmeisser K, Gems D (2017) The SKN-1/Nrf2 transcription factor can protect against oxidative stress and increase lifespan in C. elegans by distinct mechanisms. Aging Cell 16:1191–1194PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Inoue H, Jisamoto N, An JH, Oliveira RP, Nishida E, Blackwell TK, Matsumoto K (2005) The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes Dev 19:2278–2283PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    van der Hoeven R, McCallum KC, Cruz MR, Garsin DA (2011) Ce-Duox1/BLI-3 generated reactive oxygen species trigger protective SKN-1 activity via p38 MAPK signaling during infection in C. elegans. PLoS Pathog 7:e1002453PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Wu C-W, Deonarine A, Przybysz A, Strange K, Choe KP (2016) The Skp1 homologs SKR-1/2 are required for the Caenorhabditis elegans SKN-1 antioxidant/detoxification response independently of p38 MAPK. PLoS Genet 12:e1006361PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Hu Q, D’Amora DR, Macneil LT, Walhout AJM, Kubiseski TJ (2017) The oxidative stress response in Caenorhabditis elegans requires the GATA transcription factor ELT-3 and SKN-1/Nrf2. Genetics 206:1909–1922PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    An JH, Vranas K, Lucke M, Inoue H, Hisamoto N, Matsomoto K, Blackwekk TK (2005) Regulation of the Caenorhabditis elegans oxidative stress defense protein SKN-1 by glycogen synthase kinase-3. Proc Natl Acad Sci USA 102:16275–16280PubMedCrossRefGoogle Scholar
  34. 34.
    Goh GYS, Marteli KL, Parhar KS, Kwong AWL, Wong MA, Mah A, Hou NS, Taubert S (2014) The conserved mediator subunit MDT-15 is required for oxidative stress responses in Caenorhabditis elegans. Aging Cell 13:70–79PubMedCrossRefGoogle Scholar
  35. 35.
    Kell A, Ventura N, Kahn N, Johnson TE (2007) Activation of SKN-1 by novel kinases in Caenorhabditis elegans. Free Radic Biol Med 43:1560–1566PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Hourihan JM, Mazzeo LEM, Femandez-Cardenas LP, Blackwell TK (2016) Cysteine sulfenylation directs IRE-1 to activate the SKN-1/Nrf2 antioxidant response. Mol Cell 63:553–566PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Rizki G, Picard CL, Pereyra C, Lee SS (2012) Host cell factor 1 inhibits SKN-1 to modulate oxidative stress responses in Caenorhabditis elegans. Aging Cell 11:717–721PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Kim Y, Sun H (2007) Functional genomic approach to identify novel genes involved in the regulation of oxidative stress resistance and animal lifespan. Aging Cell 6:489–503PubMedCrossRefGoogle Scholar
  39. 39.
    Wu Q-L, Zhao Y-L, Li Y-P, Wang D-Y (2014) Molecular signals regulating translocation and toxicity of graphene oxide in nematode Caenorhabditis elegans. Nanoscale 6:11204–11212PubMedCrossRefGoogle Scholar
  40. 40.
    Wu Q-L, Yin L, Li X, Tang M, Zhang T, Wang D-Y (2013) Contributions of altered permeability of intestinal barrier and defecation behavior to toxicity formation from graphene oxide in nematode Caenorhabditis elegans. Nanoscale 5(20):9934–9943PubMedCrossRefGoogle Scholar
  41. 41.
    Ding X-C, Wang J, Rui Q, Wang D-Y (2018) Long-term exposure to thiolated graphene oxide in the range of μg/L induces toxicity in nematode Caenorhabditis elegans. Sci Total Environ 616–617:29–37PubMedCrossRefGoogle Scholar
  42. 42.
    Li Y-X, Wang W, Wu Q-L, Li Y-P, Tang M, Ye B-P, Wang D-Y (2012) Molecular control of TiO2-NPs toxicity formation at predicted environmental relevant concentrations by Mn-SODs proteins. PLoS ONE 7(9):e44688PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Li Y-X, Yu S-H, Wu Q-L, Tang M, Pu Y-P, Wang D-Y (2012) Chronic Al2O3-nanoparticle exposure causes neurotoxic effects on locomotion behaviors by inducing severe ROS production and disruption of ROS defense mechanisms in nematode Caenorhabditis elegans. J Hazard Mater 219–220:221–230PubMedCrossRefGoogle Scholar
  44. 44.
    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 8:14102PubMedCrossRefGoogle Scholar
  45. 45.
    Zhi L-T, Qu M, Ren M-X, Zhao L, Li Y-H, Wang D-Y (2017) Graphene oxide induces canonical Wnt/β-catenin signaling-dependent toxicity in Caenorhabditis elegans. Carbon 113:122–131CrossRefGoogle Scholar
  46. 46.
    Ren M-X, Zhao L, Lv X, Wang D-Y (2017) Antimicrobial proteins in the response to graphene oxide in Caenorhabditis elegans. Nanotoxicology 11:578–590PubMedCrossRefGoogle Scholar
  47. 47.
    Zhao L, Rui Q, Wang D-Y (2017) Molecular basis for oxidative stress induced by simulated microgravity in nematode Caenorhabditis elegans. Sci Total Environ 607–608:1381–1390PubMedCrossRefGoogle Scholar
  48. 48.
    Zhao Y-L, Yang J-N, Wang D-Y (2016) A microRNA-mediated insulin signaling pathway regulates the toxicity of multi-walled carbon nanotubes in nematode Caenorhabditis elegans. Sci Rep 6:23234PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Zhi L-T, Fu W, Wang X, Wang D-Y (2016) ACS-22, a protein homologous to mammalian fatty acid transport protein 4, is essential for the control of toxicity and translocation of multi-walled carbon nanotubes in Caenorhabditis elegans. RSC Adv 6:4151–4159CrossRefGoogle Scholar
  50. 50.
    Yang R-L, Rui Q, Kong L, Zhang N, Li Y, Wang X-Y, Tao J, Tian P-Y, Ma Y, Wei J-R, Li G-J, Wang D-Y (2016) Metallothioneins act downstream of insulin signaling to regulate toxicity of outdoor fine particulate matter (PM2.5) during Spring Festival in Beijing in nematode Caenorhabditis elegans. Toxicol Res 5:1097–1105CrossRefGoogle Scholar
  51. 51.
    Zhi L-T, Ren M-X, Qu M, Zhang H-Y, Wang D-Y (2016) Wnt ligands differentially regulate toxicity and translocation of graphene oxide through different mechanisms in Caenorhabditis elegans. Sci Rep 6:39261PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Xiao G-S, Zhao L, Huang Q, Yang J-N, Du H-H, Guo D-Q, Xia M-X, Li G-M, Chen Z-X, Wang D-Y (2018) Toxicity evaluation of Wanzhou watershed of Yangtze Three Gorges Reservoir in the flood season in Caenorhabditis elegans. Sci Rep 8:6734PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    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 163:298–306PubMedCrossRefGoogle Scholar
  54. 54.
    Ding X-C, Rui Q, Wang D-Y (2018) Functional disruption in epidermal barrier enhances toxicity and accumulation of graphene oxide. Ecotoxicol Environ Saf 163:456–464PubMedCrossRefGoogle Scholar
  55. 55.
    Wang D-Y (2018) Nanotoxicology in Caenorhabditis elegans. Springer, SingaporeCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

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

Personalised recommendations