Heavy metals induce oxidative stress and trigger oxidative stress-mediated heat shock protein (hsp) modulation in the intertidal copepod Tigriopus japonicus

Comp Biochem Physiol C Toxicol Pharmacol. 2014 Nov;166:65-74. doi: 10.1016/j.cbpc.2014.07.005. Epub 2014 Jul 21.


Heat shock proteins (hsps) are induced by a wide range of environmental stressors including heavy metals in aquatic organisms. However, the effect of heavy metals on zooplankton at the molecular level remains still unclear. In this study, we measured the intracellular reactive oxygen species (ROS) level and the antioxidant enzyme activities for 96 h after exposure to five heavy metals: arsenic (As), cadmium (Cd), copper (Cu), silver (Ag), and zinc (Zn) in the intertidal copepod Tigriopus japonicus. Activities of the antioxidant enzymes were highly elevated in metal-exposed copepods, indicating that heavy metals can induce oxidative stress by generating ROS, and stimulate the involvement of antioxidant enzymes as cellular defense mechanisms. Subsequently, transcriptional changes in hsp gene families were further investigated in the metal-exposed groups for 96 h. The ROS level and glutathione (GSH) content were significantly increased in Ag-, As-, and Cu-exposed copepods, while they were only slightly elevated in Cd- and Zn-exposed groups. Based on the numbers of significantly modulated hsp genes and their expression levels for 96 h, we measured the effect of heavy metals to stress genes of T. japonicus in the following order: Cu > Zn > Ag > As > Cd, implying that Cu acts as a stronger oxidative stress inducer than other heavy metals. Of them, the expression of hsp20 and hsp70 genes was substantially modulated by exposure to heavy metals, indicating that these genes would provide a sensitive molecular biomarker for aquatic monitoring of heavy metal pollution.

Keywords: Antioxidant enzyme activities; Copepod; Heat shock protein; Heavy metal; Oxidative stress; Tigriopus japonicus.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aquaculture
  • Arthropod Proteins / agonists
  • Arthropod Proteins / genetics
  • Arthropod Proteins / metabolism
  • Biomarkers / chemistry
  • Biomarkers / metabolism
  • Copepoda / drug effects*
  • Copepoda / growth & development
  • Copepoda / metabolism
  • Dose-Response Relationship, Drug
  • Environmental Exposure / adverse effects
  • Female
  • Gene Expression Regulation, Developmental / drug effects*
  • Glutathione / agonists
  • Glutathione / genetics
  • Glutathione / metabolism
  • HSP20 Heat-Shock Proteins / agonists*
  • HSP20 Heat-Shock Proteins / genetics
  • HSP20 Heat-Shock Proteins / metabolism
  • HSP70 Heat-Shock Proteins / agonists*
  • HSP70 Heat-Shock Proteins / genetics
  • HSP70 Heat-Shock Proteins / metabolism
  • Male
  • Metals, Heavy / administration & dosage
  • Metals, Heavy / toxicity*
  • Oxidative Stress / drug effects*
  • Oxidoreductases / chemistry
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism
  • Reactive Oxygen Species / agonists
  • Reactive Oxygen Species / metabolism
  • Republic of Korea
  • Toxicity Tests, Acute
  • Water Pollutants, Chemical / administration & dosage
  • Water Pollutants, Chemical / toxicity*


  • Arthropod Proteins
  • Biomarkers
  • HSP20 Heat-Shock Proteins
  • HSP70 Heat-Shock Proteins
  • Metals, Heavy
  • Reactive Oxygen Species
  • Water Pollutants, Chemical
  • Oxidoreductases
  • Glutathione