Log in

Effect of phenol on embryo development and expression of metallothionein in the sea urchin Hemicentrotus pulcherrimus

  • Article
  • Published:
Ocean Science Journal Aims and scope Submit manuscript

Abstract

In this study, we identified and cloned the sea urchin Hemicentrotus pulcherrimus MT (Hp-MT) mRNA. We examined the gameto- and embryo-toxic effects and the expression of Hp-MT mRNA at various concentrations of phenol in H. pulcherrimus. We found that the normal embryogenesis rate was significantly inhibited when H. pulcherrimus was exposed to phenol (EC50 = 1565.86 ppb, 95% Cl = 1183.47-2037.84 ppb). The no observed effective concentration (NOEC) and the lowest observed effective concentration (LOEC) of the normal embryogenesis rate were < 10 ppb and 100 ppb, respectively. Hp-MT cDNA is 651 bp in length and encodes a protein of 64 amino acids. We found that the expression of Hp-MT mRNA was significantly increased with phenol treatment in a concentrationdependent manner. These results suggest that phenol at greater than 100 ppb has a toxic effect during the early embryonic stages of H. pulcherrimus, and MT mRNA may be used as a biomarker for risk assessment of phenol contamination.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson SL, Hose JE, Knezovich JP (1994) Genotoxic and developmental effects in sea urchins are sensitive indications of effects of genotoxic chemicals. Environ Toxicol Chem 13:1033–1041

    Article  Google Scholar 

  • Arslan OC, Parlak H, Oral R, Katalay S (2007) The effects of nonylphenol and octylphenol on embryonic development of sea urchin (Paracentrotus lividus). Arch Environ Con Tox 53:214–219

    Article  Google Scholar 

  • Atici T, Ahisks S, Altindag A, Aydin D (2008) Ecological effects of some heavy metals (Cd, Pb, Hg, Cr) pollution of phytoplanktonic algae and zooplanktonic organisms in Sariyar Dam Reservoir in Turkey. Afr J Biotechnol 7:1972–1977

    Google Scholar 

  • Au DWT, Chiang MWL, Wu RSS (2000) Effects of cadmium and phenol on motility and ultrastructure of sea urchin and mussel spermatozoa. Arch Environ Con Tox 38:455–463

    Article  Google Scholar 

  • Au DWT, Yurchenko OV, Reunov AA (2003) Sublethal effects of phenol on spermatogenesis in sea urchins (Anthocidaris crassispina). Environ Res 93:92–98

    Article  Google Scholar 

  • Bachman MJ, Keller JM, West KL, Jensen BA (2014) Persistent organic pollutant concentrations in blubber of 16 species of cetaceans stranded in the Pacific Islands from 1997 through 2011. Sci Total Environ 488–489:115–123

    Article  Google Scholar 

  • Bielmyer GK, Brix KV, Capo TR, Grosell M (2005) The effects of metals on embryo-larval and adult life stages of the sea urchin, Diadema antillarum. Aquat Toxicol 74:254–263

    Article  Google Scholar 

  • Bourdineaud JP, Baudrimont M, Gonzalez P, Moreau JL (2006) Challenging the model for induction of metallothionein gene expression. Biochimie 88:1787–1792

    Article  Google Scholar 

  • Buttino I (1994) The effect of low concentrations of phenol and ammonia on egg production rates, fecal pellet production and egg viability of the calanoid copepod Acartia clausi. Mar Biol 119:629–634

    Article  Google Scholar 

  • Cai L, Satoh M, Tohyama C, Cherian MG (1999) Metallothionein in radiation exposure: its induction and protective role. Toxicology 132:85–98

    Article  Google Scholar 

  • Canesi L, Lorusso LC, Ciacci C, Betti M, Rocchi M, Pojana G, Marcomini A (2007) Immunomodulation of Mytilus hemocytes by individual estrogenic chemicals and environmentally relevant mixtures of estrogens: in vitro and in vivo studies. Aquat Toxicol 81:36–44

    Article  Google Scholar 

  • Cavaletto M, Ghezzi A, Burlando B, Evangelisti V, Ceratto N, Viarengo A (2002) Effect of hydrogen peroxide on antioxidant enzymes and metallothionein level in the digestive gland of Mytilus galloprovincialis. Comp Biochem Phys C 131:447–455

    Google Scholar 

  • Cavalieri V, Spinelli G (2014) Early asymmetric cues triggering the dorsal/ventral gene regulatory network of the sea urchin embryo. Elife 3:e04664

    Article  Google Scholar 

  • Chaube R, Gautam GJ, Joy KP (2013) Teratogenic effects of 4- nonylphenol on early embryonic and larval development of the catfish Heteropneustes fossilis. Arch Environ Con Tox 64:554–561

    Article  Google Scholar 

  • Cosson RP (1994) Heavy metals intracellular balance and relationships with metallothionein induction in the liver of carp after contamination by silver, cadmium and mercury following or not pretreatment by zinc. Biometals 7:9–19

    Article  Google Scholar 

  • Cui M, Siriwon N, Li E, Davidson EH, Peter IS (2014) Specific functions of the Wnt signaling system in gene regulatory networks throughout the early sea urchin embryo. P Natl Acad Sci USA 111:E5029–E5038

    Article  Google Scholar 

  • DeForest DK, Brix KV, Adams WJ (2007) Assessing metal bioaccumulation in aquatic environments: the inverse relationship between bioaccumulation factors, trophic transfer factors and exposure concentration. Aquat Toxicol 84:236–246

    Article  Google Scholar 

  • Guinot D, Urena R, Pastor A, Varo I, del Ramo J, Torreblanca A (2012) Long-term effect of temperature on bioaccumulation of dietary metals and metallothionein induction in Sparus aurata. Chemosphere 87:1215–1221

    Article  Google Scholar 

  • Habibi-Yangjeh A, Danandeh-Jenagharad M, Nooshyar M (2006) Application of artificial neural networks for predicting the aqueous acidity of various phenols using QSAR. J Mol Model 12:338–347

    Article  Google Scholar 

  • Holcombe GW, Phipps GL, Fiandt JT (1982) Effects of phenol, 2,4-dimethylphenol, 2, 4-dichlorophenol, and pentachlorophenol on embryo, larval, and early juvenile fathead minnows (Pimephales promelas). Arch Environ Con Tox 11:73–78

    Article  Google Scholar 

  • Hwang UK, Park JS, Kwon JN, Heo S, Oshima Y, Kang HS (2012) Effect of nickel on embryo development and expression of metallothionein gene in the sea urchin (Hemicentrotus pulcherrimus). J Fac Agr Kyushu U 57:145–149

    Google Scholar 

  • Kim JH, Rhee, JS, Dahms HU, Lee YM, Han KN, Lee JS (2012) The yellow catfish, Pelteobagrus fulvidraco (Siluriformes) metallothionein cDNA: molecular cloning and transcript expression level in response to exposure to the heavy metals Cd, Cu, and Zn. Fish Physiol Biochem 38:1331–1342

    Article  Google Scholar 

  • Kobayashi N (1980) Comparative sensitivity of various developmental stages of sea urchins to some chemicals. Mar Biol 58:163–171

    Article  Google Scholar 

  • Kowalska K, Bizon A, Zalewska M, Milnerowicz H (2015) The influence of biological and environmental factors on metallothionein concentration in the blood. J Trace Elem Med Bio 29:99–103

    Article  Google Scholar 

  • LeBlanc GA, Mu X, Rider CV (2000) Embryotoxicity of the alkylphenol degradation product 4-nonylphenol to the crustacean Daphnia magna. Environ Health Perspt 108:1133–1138

    Article  Google Scholar 

  • Lee SH (2006) Differential gene expression in nickel (II)-treated normal rat kidney cells. Res Commun Mol Path 119:77–87

    Google Scholar 

  • Liu Y, Wu H, Yu Z, Guo Y, Zhang J, Zhu KY, Ma E (2015) Transcriptional response of two metallothionein genes (OcMT1 and OcMT2) and histological changes in Oxya chinensis (Orthoptera: Acridoidea) exposed to three trace metals. Chemosphere 139:310–317

    Article  Google Scholar 

  • Ma W, He Y, Yan T, Wang L (2014) Tissue-specific copper accumulation, zinc levels, induction, and purification of metallothionein in freshwater crab Sinopotamon henanense exposed to subacute waterborne copper. Environ Toxicol 29:407–417

    Article  Google Scholar 

  • Malaysia DOE-MU (1986) Water quality criteria and standards for Malaysia, vol. 4 - criteria and standards for organic constituents. Malaysia Department of Environment, University of Malaya, 224 p

    Google Scholar 

  • Marshall DJ (2006) Reliably estimating the effect of toxicants on fertilization success in marine broadcast spawners. Mar Pollut Bull 52:734–738

    Article  Google Scholar 

  • Michalowicz J, Duda W (2007) Phenols - sources and toxicity. Pol J of Environ Stud 16:347–362

    Google Scholar 

  • Miles AT, Hawksworth GM, Beattie JH, Rodilla V (2000) Induction, regulation, degradation and biological significance of mammalian metallothioneins. Crit Rev Biochem Mol 35:35–70

    Article  Google Scholar 

  • Monroy A (1986) A centennial debt of developmental biology to the sea urchin. Biol Bull 171:509–519

    Article  Google Scholar 

  • Oguro T, Yoshida T (2001) Effect of ultraviolet A on ornithine decarboxylase and metallothionein gene expression in mouse skin. Photodermatol Photo 17:71–78

    Article  Google Scholar 

  • Paintner R, Howard R (1982) The Hela DNA-synthesis inhibition test as a rapid screen for mutagenic carcinogens. Mutat Res 92:427–437

    Article  Google Scholar 

  • Paul-Pont I, Gonzalez P, Montero N, de Montaudouin X, Baudrimont M (2012) Cloning, characterization and gene expression of a metallothionein isoform in the edible cockle Cerastoderma edule after cadmium or mercury exposure. Ecotox Environ Safe 75:119–126

    Article  Google Scholar 

  • Pérez J, Dominiques I, Monterio M, Soares AM, Loureiro S (2013) Synergistic effects caused by atrazine and terbuthylazine on chlorpyrifos toxicity to early-life stages of the zebrafish Danio rerio. Environ Sci Pollut R 20:4671–4680

    Article  Google Scholar 

  • Perrault JR (2014) Mercury and selenium ingestion rates of Atlantic leatherback sea turtles (Dermochelys coriacea): a cause for concern in this species? Mar Environ Res 99:160–169

    Article  Google Scholar 

  • Russo R, Bonaventura R, Zito F, Schröder HC, Müller I, Müller WEG, Matranga V (2003) Stress to cadmium monitored by metallothionein gene induction in Paracentrotus lividus embryos. Cell Stress Chaperon 8:232–241

    Article  Google Scholar 

  • Saha NC, Bhunia F, Kaviraj A (1999) Toxicity of phenol to fish and aquatic ecosystems. B Environ Contam Tox 63:195–202

    Article  Google Scholar 

  • Stringer TJ, Glover CN, Keesing V, Northcott GL, Tremblay LA (2012) Development of a harpacticoid copepod bioassay: selection of species and relative sensitivity to zinc, atrazine and phenanthrene. Ecotox Environ Safe 80:363–371

    Article  Google Scholar 

  • Takaishi M, Sawada M, Shimada A, Suzuki JS, Satoh M, Nagase H (2009) Protective role of metallothionein in benzo(a)pyreneinduced DNA damage. J Toxicol Sci 34:449–458

    Article  Google Scholar 

  • Theocharis SE, Margeli AP, Koutselinis A (2003) Metallothionein: a multifunctional protein from toxicity to cancer. Int J Biol Marker 18:162–169

    Google Scholar 

  • USEPA (1987) Quality criteria for water 1986. US Environment Protection Agency, Washington DC, US Environment Protection Agency Report 440/5-86-001, 453 p

    Google Scholar 

  • van Heijster P, Hardway H, Kaper TJ, Bradham CA (2014) A computational model for BMP movement in sea urchin embryos. J Theor Biol 363:277–289

    Article  Google Scholar 

  • Verma SR, Rani S, Tyagi AK, Dalela RC (1980) Evaluation of acute toxicity of phenol and its chloro-and nitro-derivatives to certain teleosts. Water Air Soil Poll 14:95–102

    Article  Google Scholar 

  • Viarengo A, Burlando B, Ceratto N, Panfoli I (2000) Antioxidant role of metallothioneins: a comparative overview. Cell Mol Biol 46:407–417

    Google Scholar 

  • Volpi Ghirardini A, Arizzi Novelli A (2001) A sperm cell toxicity test procedure for the Mediterranean species Paracentrotus lividus (Echinodermata: Echinoidea). Environ Technol 22:439–445

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Han Seung Kang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hwang, UK., Lee, JW., Ryu, HM. et al. Effect of phenol on embryo development and expression of metallothionein in the sea urchin Hemicentrotus pulcherrimus . Ocean Sci. J. 50, 701–708 (2015). https://doi.org/10.1007/s12601-015-0063-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12601-015-0063-8

Keywords

Navigation