Skip to main content
SpringerLink
Log in

Comparative responses of Sinopotamon henanense to acute and sub-chronic Cd exposure

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Studies on the freshwater crab Sinopotamon henanense have shown that acute and sub-chronic Cd2+ exposure induced differential alterations in the respiratory physiology and gill morphology. To elucidate Cd2+ toxicity under these two exposure conditions, crabs were acutely exposed to 7.14, 14.28, and 28.55 mg/L Cd2+ for 96 h and sub-chronically exposed to 0.71, 1.43, and 2.86 mg/L Cd2+ for 3 weeks. The Cd2+ accumulation, total metallothionein (MT), superoxide dismutase, and malondialdehyde (MDA) contents in the gill tissues were detected. Moreover, the glucose-6-phosphate dehydrogenase (G6PDH) activity, NADPH content, reduced glutathione (GSH), oxidized glutathione (GSSG), and GSH/GSSG ratio in the hepatopancreas were determined. The morphology of the X-organ–sinus gland complex was also observed. The results showed that sub-chronical Cd2+ exposure induced lower MT content and higher MDA level in the gills than in the acute exposure. In the hepatopancreas, acute Cd2+ exposure decreased the pentose phosphate pathway activity and NADPH content; however, an increased G6PDH activity and NADPH content were detected in sub-chronic Cd2+ exposure (2.86 mg/L). Morphological changes occurred in the sinus gland in crabs exposed to 2.86 mg/L Cd2+ for 3 weeks. The tightly packed structure composed by the axons, enlarged terminals, and glial cells, became loose and porous. Ultra-structurally, a large number of vacuoles and few neurosecretory granules were observed in the axon terminal. These effects added to our understanding of the toxic effects of Cd2+ and provide biochemical and histopathological evidence for S. henanense as a biomarker of acute or long-term waterborne Cd2+ pollution.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The data sets used and analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Atli G, Canli M (2010) Response of antioxidant system of freshwater fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicol Environ Saf 73:1884–1889

    Article  CAS  Google Scholar 

  • Böcking D, Dircksen H, Keller R (2002) The crustacean neuropeptides of the CHH/MIH/GIH family: structures and biological activities. In: Wiese K (ed) The Crustacean Nervous System. Springer, Berlin, pp 84–97

    Chapter  Google Scholar 

  • Cheng L, Zhou JL, Cheng J (2018) Bioaccumulation, tissue distribution and joint toxicity of erythromycin and cadmium in Chinese mitten crab (Eriocheir sinensis). Chemosphere 210:267–278

    Article  CAS  Google Scholar 

  • Chung JS, Webster SG (2005) Dynamics of in vivo release of molt-inhibiting hormone and crustacean hyperglycemic hormone in the shore crab, Carcinus maenas. Endocrinology 146:5545–5551

    Article  CAS  Google Scholar 

  • Chung JS, Zmora N (2008) Functional studies of crustacean hyperglycemic hormone (CHHs) of the blue crab, Callinectes sapidus-the expression and release of CHH in eyestalk and pericardial organ in response to environmental stress. FEBS J 275:693–704

    Article  CAS  Google Scholar 

  • Chung JS, Bembe S, Tamone S (2009) Molecular cloning of the crustacean hyperglycemic hormone (CHH) precursor from the X-organ and the identification of the neuropeptide from sinus gland of the Alaskan Tanner crab, Chionoecetes bairdi. Gen Comp Endocrinol 162:129–133

    Article  CAS  Google Scholar 

  • Das S, Tseng LC, Chou C, Wang L, Souissi S, Hwang JS (2019) Effects of cadmium exposure on antioxidant enzymes and histological changes in the mud shrimp Austinogebia edulis (Crustacea: Decapoda). Environ Sci Pollut Res Int 26(8):7752–7762

    Article  CAS  Google Scholar 

  • Diaz-Flores M, Ibanez-Hernandez MA, Galvan RE (2006) Glucose-6-phosphate dehydrogenase activity and NADPH/NADP+ ratio in liver and pancreas are dependent on the severity of hyperglycemia in rat. Life Sci 78:2601–2607

    Article  CAS  Google Scholar 

  • Duangprom S, Kornthong N, Suwansaard S, Srikawnawan W, Chotwiwatthanakun C, Sobhon P (2017) Distribution of crustacean hyperglycemic hormones (CHH) in the mud crab (Scylla olivacea) and their differential expression following serotonin stimulation. Aquacultrue 468:481–488

    Article  CAS  Google Scholar 

  • He Y, Wang L, Ma W, Lu X, Li Y, Liu J (2019) Secretory expression, immunoaffinity purification and metal-binding ability of recombinant metallothionein (ShMT) from freshwater crab Sinopotamon henanense. Ecotoxicol Environ Saf 169:457–463

    Article  CAS  Google Scholar 

  • Irato P, Santovito G, Piccinni E (2001) Oxidative burst and metallothionein as a scavenger in macrophages. Immunol Cell Biol 79:251–254

    Article  CAS  Google Scholar 

  • Jing W, Lang L, Lin Z, Liu N, Wang L (2019) Cadmium bioaccumulation and elimination in tissues of the freshwater mussel Anodonta woodiana. Chemosphere 219:321–327

    Article  CAS  Google Scholar 

  • Kim BM, Jeong CB, Han J, Kim IC, Rhee JS, Lee JS (2013) Role of crustacean hyperglycemic hormone (CHH) in the environmental stressor-exposed intertidal copepod Tigriopus japonicus. Comp Biochem Physiol 158C:131–141

    Google Scholar 

  • Klaassen CD, Liu J, Diwan BA (2009) Metallothionein protection of cadmium toxicity. Toxicol Appl Pharmacol 238(3):215–220

    Article  CAS  Google Scholar 

  • Lange A, Ausseil O, Segener H (2002) Alterations of tissue glutathione levels and metallothionein mRNA rainbow in trout during single and combined exposure to cadmium and zinc. Comp Biochem Physiol 131C:231–243

    CAS  Google Scholar 

  • Lei W, Wang L, Liu D (2011) Histopathological and biochemical alterations of the heart induced by acute cadmium exposure in the freshwater crab Sinopotamon yangtsekiense. Chemosphere 84:689–694

    Article  CAS  Google Scholar 

  • Li Y, Wang L, Liu N, Wang Q, He Y, Meng F (2008) Effects of cadmium on enzyme activity and lipid peroxidation of Sinopotamon yangtsekiense. Acta Hydrobiologica Sinica 3:373–379

    Article  Google Scholar 

  • Li N, Hou YH, Ma DD, Jing WX, Dahms HU, Wang L (2015a) Lead accumulation, oxidative damage and histopathological alteration in testes and accessory glands of freshwater crab, Sinopotamon henanense, induced by acute lead exposure. Ecotoxicol Environ Saf 117:20–27

    Article  CAS  Google Scholar 

  • Li Y, Wu H, Wei X, He Y, Li B, Li Y, Jing W, Wang L (2015b) Subcellular distribution of Cd and Zn and MT mRNA expression in the hepatopancreas of Sinopotamon henanense after single and co-exposure to Cd and Zn. Comp Biochem Physiol 167C:117–130

    Google Scholar 

  • Liu N, Yan B, Li Y, Wang L (2008) The effect of Cd2+ on the glutathione system of the freshwater crab Sinopotamon yangtsekiense. Environ Sci 29(8):2302–2307

    CAS  Google Scholar 

  • Liu A, Liu J, Chen X, Lu B, Zeng C, Ye H (2019) A novel crustacean hyperglycemic hormone (CHH) from the mud crab Scylla paramamosa in regulating carbohydrate metabolism. Comp Biochem Physiol 231A:49–55

    Article  CAS  Google Scholar 

  • Lorenzon S, Francese M, Ferrero EA (2000) Heavy metal toxicity and differential effects on the hyperglycemic stress response in the shrimp Palaemon elegans. Arch Environ Contam Toxicol 39:167–176

    Article  CAS  Google Scholar 

  • Ma W, Wang L, He Y (2008) Tissue-specific cadmium and metallothionein levels in freshwater crab Sinopotamon henanense during acute exposure to waterborne cadmium. Environ Toxicol 23:393–400

    Article  CAS  Google Scholar 

  • Martinez-Finley EJ, Aschner M (2011) Revelations from the nematode Caenorhabditis elegans on the complex interplay of metal toxicological mechanisms. J Toxicol. https://doi.org/10.1155/2011/895236

  • Matić D, Vlahović M, Ilijin L, Mrdaković M, Grčić A, Filipović A, Perićeri oviić V (2020) Metallothionein level, non-specific esterases, fitness-related traits and integrated biomarker response (IBR) in larvae of Lymantria dispar (Lepidoptera) originating from unpolluted and polluted locations after chronic cadmium treatment. Ecol Indic 112:106136

  • May BA, Golding DW (1983) Aspects of secretory phenomena within the sinus gland of Carcinus maenas (L.). Cell Tissue Res 228:245–254

    Article  CAS  Google Scholar 

  • Medesani DA, López Greco LS, Rodríguez EM (2001) Effects of cadmium and copper on hormonal regulation of glycemia by the eyestalks, in the crab Chasmagnathus granulata. Bull Environ Contam Toxicol 66:71–76

    Article  CAS  Google Scholar 

  • Medesani DA, López Greco LS, Rodríguez EM (2004) Disruption of endocrine regulation of glycemia levels by cadmium and copper in the estuarine crab Chasmagnathus granulata. Bull Environ Contam Toxicol 73:942–946

    Article  CAS  Google Scholar 

  • Pedersen KL, Bach LT, Bjerregaard P (2014) Amount and metal composition of midgut gland metallothionein in shore crabs (Carcinus maenas) after exposure to cadmium in the food. Aquat Toxicol 150:182–188

    Article  CAS  Google Scholar 

  • Pierron F, Baudrimont M, Bossy A (2007) Impairment of lipid storage by cadmium in the European eel (Anguilla anguilla). Aquat Toxicol 81:304–311

    Article  CAS  Google Scholar 

  • Rhee JS, Yu IT, Kim BM, Jeong CB, Lee KW, Kim MJ, Lee SJ, Park GS, Lee JS (2013) Copper induces apoptotic cell death through reactive oxygen species-triggered oxidative stress in the intertidal copepod Tigriopus japonicus. Aquat Toxicol 132-133:182–189

    Article  CAS  Google Scholar 

  • Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30:1191–1212

    Article  CAS  Google Scholar 

  • Schuwerack PMM, Lewis JW (2003) Cellular responses to increasing Cd concentrations in the freshwater crab, Potamonautes warreni, harbouring microbial gill infestations. Cell Tissue Res 313:335–346

    Article  CAS  Google Scholar 

  • Silvestre F, Duchêne C, Trausch G (2005) Tissue-specific cadmium accumulation and metallothionein-like protein levels during acclimation process in the Chinese crab Eriocheir sinensis. Comp Biochem Physiol 140 C:39–45

    Google Scholar 

  • Sook Chung J, Christie A, Flynn E (2020) Molecular cloning of crustacean hyperglycemic hormone (CHH) family members (CHH, molt-inhibiting hormone and mandibular organ-inhibiting hormone) and their expression levels in the Jonah crab, Cancer borealis. Gen Comp Endocrinol 295:113522. https://doi.org/10.1016/j.ygcen.2020.113522.

  • Sun J, Liu A, Du Y (2001) Microscopic and ultrastructure of sinus glands of Eriocheir sinensis. Acta Zool Sin 47:27–31

    Google Scholar 

  • Thornalley P, Vâsàk M (1985) Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochim Biophys Acta 827:36–44

    Article  CAS  Google Scholar 

  • Tian WN, Braunstein LD, Apse K (1999) Importance of glucose-6-phosphate dehydrogenase activity in cell death. Am J Phys Cell Phys 276:C1121–C1131

    CAS  Google Scholar 

  • Vijayavel K, Balasubramanian MP (2006) Changes in oxygen consumption and respiratory enzymes as stress indicators in an estuarine edible crab Scylla serrata exposed to naphthalene. Chemosphere 63:1523–1531

    Article  CAS  Google Scholar 

  • Wang L, Yan B, Liu N (2008) Effects of cadmium on glutathione synthesis in hepatopancreas of freshwater crab, Sinopotamon yangtsekiense. Chemosphere 74:51–56

    Article  CAS  Google Scholar 

  • Wang L, Xu T, Lei W (2011) Cadmium-induced oxidative stress and apoptotic changes in the testis of freshwater crab, Sinopotamon henanense. PLoS One 6:1–8

    Google Scholar 

  • Webster SG, Keller R, Dircksen H (2012) The CHH-superfamily of multifunctional peptide hormones controlling crustacean metabolism, osmoregulation, moulting, and reproduction. Gen Comp Endocrinol 175:217–233

    Article  CAS  Google Scholar 

  • Winzer K, VanNoorden CJF, Kohler A (2002) Glucose-6-phosphate dehydrogenase: the key to sex-related xenobiotic toxicity in hepatocytes of European flounder (Platichthys flesus L.)? Aquat Toxicol 56:275–288

    Article  CAS  Google Scholar 

  • Xu P, Guo H, Wang H (2019a) Identification and profiling of microRNAs responsive to cadmium toxicity in hepatopancreas of the freshwater crab Sinopotamon henanense. Hereditas 156:34

    Article  Google Scholar 

  • Xu L, Pan L, Zhang X, Wei C (2019b) Effects of crustacean hyperglycemic hormone (CHH) on regulation of hemocyte intracellular signaling pathways and phagocytosis in white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 93:559–566

    Article  CAS  Google Scholar 

  • Xuan R, Wu H, Lin C, Ma D, Li Y, Xu T, Wang L (2013) Oxygen consumption and metabolic responses of freshwater crab Sinopotamon henanense to acute and sub-chronic cadmium exposure. Ecotoxicol Environ Saf 89:29–35

    Article  CAS  Google Scholar 

  • Xuan R, Wu H, Li Y, Wang J, Wang L (2014) Sublethal Cd-induced cellular damage and metabolic changes in the freshwater crab Sinopotamon henanense. Environ Sci Pollut Res 21(3):1738–1745

    Article  CAS  Google Scholar 

  • Yang HZ, Gu WJ, Chen W, Hwang JS, Wang L (2019) Metal binding characterization of heterologously expressed metallothionein of the freshwater crab Sinopotamon henanense. Chemosphere 235:926–934

    Article  CAS  Google Scholar 

  • Yang HZ, Wang L, He YJ, Jing WX, Ma WL, Chen CM, Wang L (2020) Analysis of spectrometry and thermodynamics of the metallothionein in freshwater crab Sinopotamon henanense for its binding ability with different metals. Chemosphere 246:125670. https://doi.org/10.1016/j.chemosphere.2019.125670

    Article  CAS  Google Scholar 

  • Yu D, Peng X, Ji C, Li F, Wu H (2020) Metal pollution and its biological effects in swimming crab Portunus trituberculatus by NMR-based metabolomics. Mar Pollut Bull 157:111307

    Article  CAS  Google Scholar 

  • Zhang X, Pan L, Wei C, Tong R, Li Y, Ding M, Wang H (2020) Crustacean hyperglycemic hormone (CHH) regulates the ammonia excretion and metabolism in white shrimp, Litopenaeus vannamei under ammonia-N stress. Sci Total Environ 723:138128

    Article  CAS  Google Scholar 

  • Zhou Y, Dahms HU, Dong F, Jing W, Wang L (2016) Immune-associated parameters and antioxidative responses to cadmium in the freshwater crab Sinopotamon henanense. Ecotoxicol Environ Saf 129:235–241

    Article  CAS  Google Scholar 

  • Zhou Y, Jing W, Dahms HU, Hwang JS, Wang L (2017) Oxidative damage, ultrastructural alterations and gene expressions of hemocytes in the freshwater crab Sinopotamon henanense exposed to cadmium. Ecotoxicol Environ Saf 138 L:130–138 Declarations

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Editage (www.editage.cn) for English language editing.

Funding

The work was supported by the Natural Science Foundation of China (NO. 31272319), PhD Start-up Fund of Shanxi Medical University (NO. 03201552), and Youth Fund of Shanxi Medical University (NO.02201626).

Author information

Authors and Affiliations

  1. Laboratory Animal Center, Shanxi Medical University, Taiyuan, 030001, China

    Ruijing Xuan & Bingyan Wei

  2. Basic Medical School, Shanxi Medical University, Taiyuan, 030001, China

    Hao Wu

  3. School of Public Health, Shanxi Medical University, Taiyuan, 030001, China

    Yingjun Li

  4. School of Life Science, Shanxi University, Taiyuan, 030006, China

    Lan Wang

Authors
  1. Ruijing Xuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hao Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yingjun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bingyan Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

R.X participated in each experiment in the present study and completed the writing of the manuscript; H.W participated in the histological and ultra-structural examination of the X organ-sinus gland complex; Y. L participated in the determination of cadmium accumulation and MT content in the gill; B.W participated in the analysis of the data. The design, execution, data analysis of all experiments in this study, and manuscript writing and revision were completed under the guidance of L.W. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Lan Wang.

Ethics declarations

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Bruno Nunes

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xuan, R., Wu, H., Li, Y. et al. Comparative responses of Sinopotamon henanense to acute and sub-chronic Cd exposure. Environ Sci Pollut Res 28, 35038–35050 (2021). https://doi.org/10.1007/s11356-021-13230-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-13230-z

Keywords

Search

Navigation