Skip to main content
SpringerLink
Log in

Does a short-term exposure to cadmium chloride affects haemocyte parameters of the marine gastropod Haliotis tuberculata?

  • Molecular and cellular effects of contamination in aquatic ecosystems
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In this study, a model based on primary cultured haemocytes from the gastropod mollusc Haliotis tuberculata was established to investigate the effects of cadmium chloride in vitro. Cells were exposed for 24 h to CdCl2 concentrations of 0, 1 and 100 μg ml−1. The effects of cadmium on haemocyte parameters were investigated using morphological, spectrophotometric and flow cytometry analysis. Results showed that cadmium has no significant effects on cell viability and phagocytotic activity under the tested conditions. However, haemocytes became more rounded after cadmium exposure, which could explain the significant decrease of cell area beginning at 1 μg ml−1 of CdCl2.

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

Similar content being viewed by others

References

  • Anderson RS (1993) Modulation of non specific immunity by environmental stressors. In: Advances in fisheries science, pathobiology of marine and estuarine organisms (ed. by JA Couch and JW Fournie), pp. 483–510. CRC Press, Boca Raton, FL, USA

  • Auffret M, Rousseau S, Boutet I, Tanguy A, Baron J, Moraga D, Duchemin M (2006) A multiparametric approach for monitoring immunotoxic responses in mussels from contaminated sites in western Mediterranean. Ectotoxicol Environ Saf 63:393–405

    Article  CAS  Google Scholar 

  • Bachère E, Chargot D, Grizel H (1988) Separation of Crassostrea gigas hemocytes by density gradient centrifugation and counterflow centrifugal elutriation. Dev Comp Immunol 12:549–559

    Article  Google Scholar 

  • Banakou E, Dailianis S (2010) Involvement of Na+/H + exchanger and respiratory burst enzymes NADPH oxidase and NO synthase, in Cd-induced lipid peroxidation and DNA damage in haemocytes of mussels. Comp Biochem Physiol C 152:346–352

    Google Scholar 

  • Bossy SF, Culley MB (1976) Abalone fishing in Britain’s channel islands. Fish News Int 15:55–62

    Google Scholar 

  • Brousseau P, Pellerin J, Morin Y, Cyr D, Blakley B, Boermans H, Fournier M (2000) Flow cytometry as a tool to monitor the disturbance of phagocytosis in the clam Mya arenaria hemocytes following in vitro exposure to heavy metals. Toxicology 142:145–156

    Article  CAS  Google Scholar 

  • Chiffoleau JF, Gonzalez JL, Miramand P, Thouvenin B (2001) Le cadmium: comportement d’un contaminant métallique en estuaire. Programme Scientifique Seine Aval, 10. Ifremer, Paris.

  • Chora S, Starita-Geribaldi M, Guigonis JM, Samson M, Roméo M, Bebianno MJ (2009) Effect of cadmium in the clam Ruditapes decussatus assessed by proteomic analysis. Aquat Toxicol 94:300–308

    Article  CAS  Google Scholar 

  • Cima F, Marin MG, Matozzo V, Da Ros L, Ballarin L (1999) Biomarkers for TBT immunotoxicity studies on the cultivated clam Tapes philippinarum (Adams and Reeve, 1850). Mar Pollut Bull 39:112–115

    Article  CAS  Google Scholar 

  • Clavier J (1992) The ormer (Haliotis tuberculata) fishery of France and the Channel Islands. In: Shepherd SA, Tegner MJ, Guzman Del Proo SA (eds) Abalone of the world: biology, fisheries and culture. Fishing News Books, Oxford, pp 454–457

    Google Scholar 

  • Coles JA, Farley SR, Pipe RK (1995) Alteration of the immune response of the common marine mussel, Mytilus edulis resulting from exposure to cadmium. Dis Aquat Organ 30:367–379

    Google Scholar 

  • Crompton TR (1997) Toxicants in aqueous ecosystem. Wiley, Chichester

    Google Scholar 

  • De Guise S, Bernier J, Martineau D, Be’land P, Fournier M (1997) In vitro exposure of beluga whale lymphocytes to selected heavy metals. Environ Toxicol Chem 15:1357–1364

    Article  Google Scholar 

  • Dieter MP, Luster MI, Boorman GA, Jamieson CW, Dean JH, Cox JW (1983) Immunological and biochemical responses in mice treated with mercuric chloride. Toxicol Appl Pharmacol 68:218–228

    Article  CAS  Google Scholar 

  • Domart-Coulon I, Doumenc D, Auzoux-Bordenave S, Le Fichant Y (1994) Identification of media supplements that improve the viability of primary cell cultures of Crassostrea gigas oysters. Cytotechnology 16:109–120

    Article  CAS  Google Scholar 

  • Dyrynda EA, Pipe RK, Burt GR, Ratcliffe NA (1998) Modulations in the immune defenses of mussels (Mytilus edulis) from contaminated sites in the UK. Aquat Toxicol 42:169–185

    Article  CAS  Google Scholar 

  • Fagotti A, Di Rosa I, Simoncelli F, Pipe RK, Panara F, Pascolini R (1996) The effects of copper on actin and fibronectin organization in Mytilus galloprovincialis haemocytes. Dev Comp Immunol 20:383–391

    Article  CAS  Google Scholar 

  • Ferreira AC, Costa ACS, Korn MGA (2004) Preliminary evaluation of the cadmium concentration in seawater of the Salvador city, Brazil. Microchem J 78:77–83

    Article  CAS  Google Scholar 

  • Fournier M, Cyrl D, Blakley B, Boermans H, Brousseau P (2000) Phagocytosis as a biomarker of immunotoxicity in wildlife species exposed to environmental xenobiotics. Integr Comp Biol 40:412–420

    CAS  Google Scholar 

  • Gagnaire B (2002) Environnement et immunomodulation : étude d’activités hémocytaires chez l’huître creuse. Crassostrea gigas. Stage de DES, Ifremer

    Google Scholar 

  • Galloway TS, Depledge MH (2001) Immunotoxicity in invertebrates: measurement and ecotoxicological relevance. Ecotoxicology 10:5–23

    Article  CAS  Google Scholar 

  • Gaume B, Bourgougnon N, Auzoux-Bordenave S, Roig B, Le Bot B, Bedoux G (2012) In vitro effects of triclosan and methyl-triclosan on the marine gastropod Haliotis tuberculata. Comp Biochem Physiol Toxicol Pharmacol 156:87–94

    Article  CAS  Google Scholar 

  • Girard A (1972) La reproduction de l’ormeau, Haliotis tuberculata. Rev Tray Inst Pêches Mar 36:163–184

    Google Scholar 

  • Gomez-Mendikute A, Cajaraville MP (2003) Comparative effects of cadmium, copper, paraquat and benzo[a]pyrene on the actin cytoskeleton and production of reactive oxygen species (ROS) in mussel haemocytes. Toxicol In Vitro 17:539–546

    Article  CAS  Google Scholar 

  • Gorski J, Nugegoda D (2006) Sublethal toxicity of trace metals to larvae of the blacklip abalone, Haliotis rubra. Environ Toxicol Chem 25:1360–1367

    Article  CAS  Google Scholar 

  • Hégaret H, Wikfors GH, Soudant P (2003) Flow cytometric analysis of haemocytes from eastern oysters, Crassostrea virginica, subjected to a sudden temperature elevation: II. Haemocyte functions: aggregation, viability, phagocytosis, and respiratory burst. J Exp Mar Biol Ecol 293:249–265

    Article  Google Scholar 

  • Hooper C, Day R, Slocombe R, Handlinger J, Benkendorff K (2007) Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish Shellfish Immunol 22:363–379

    Article  CAS  Google Scholar 

  • Langston WJ, Bebianno MJ (1998) Metal metabolism in aquatic environments. In: Depledge MH, Sanders B (eds) Ecotoxicology, Series 7. Chapman and Hall, London

    Google Scholar 

  • Latire T, Le Pabic C, Mottin E, Mottier A, Costil K, Koueta N, Lebel JM, Serpentini A (2012) Responses of primary cultured haemocytes from the marine gastropod Haliotis tuberculata under 10-day exposure to cadmium chloride. Aquat Toxicol 109:213–221

    Article  CAS  Google Scholar 

  • Lebel JM, Giard W, Favrel P, Boucaud-Camou E (1996) Effects of different vertebrate growth factors on primary cultures of hemocytes from the gastropod mollusc, Haliotis tuberculata. Biol Cell 86:67–72

    Article  CAS  Google Scholar 

  • Lowe DM, Pipe RK (1994) Contaminant induced lysosomal membrane damage inmarine mussel digestive cells: an in vitro study. Aquat Toxicol 30:357–365

    Article  CAS  Google Scholar 

  • Lowe DM, Soverchiab C, Moore MN (1995) Lysosomal membrane responses in the blood 593 and digestive cells of mussels experimentally exposed to fluoranthene. Aquat Toxicol 33:105–112

    Article  CAS  Google Scholar 

  • Marigomez JA, Cajaraville MP, Angulo E (1990) Cellular cadmium distribution in the common winkle, Littorina littorea (L.) determined by X-ray microprobe analysis and histochemistry. Histochemistry 94:191–199

    Article  CAS  Google Scholar 

  • Mason AZ (1983) The uptake, accumulation and excretion of metals by the marine prosobranch gastropod mollusc Littorina littorea (L.). PhD thesis, University College of Wales, Gwymedd

  • Matozzo V, Ballarin L, Pampanin DM, Marin MG (2001) Effects of copper and cadmium exposure on functional responses of hemocytes in the clam, Tapes philippinarum. Arch Environ Contam Toxicol 41:163–170

    Article  CAS  Google Scholar 

  • McIntosh LM, Robinson WE (1999) Cadmium turnover in the hemocytes of Mercenaria mercenaria (L.) in relation to hemocyte turnover. Comp Biochem Physiol C 123:61–66

    Article  CAS  Google Scholar 

  • Moore MN, Allen JI, McVeigh A (2006) Environmental prognostics: an integrated model supporting lysosomal stress responses as predictive biomarkers of animal health status. Mar Environ Res 61:278–304

    Article  CAS  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  CAS  Google Scholar 

  • Mottin E, Caplat C, Mahaut ML, Costil K, Barillier D, Lebel JM, Serpentini A (2010) Effect of in vitro exposure to zinc on immunological parameters of haemocytes from the marine gastropod Haliotis tuberculata. Fish Shellfish Immunol 29:846–853

    Article  CAS  Google Scholar 

  • Olabarrieta I, L’Azou B, Yuric S, Cambar J, Cajaraville MP (2001) In vitro effects of cadmium on two different animal cell models. Toxicol in Vitro 15:511–517

    Article  CAS  Google Scholar 

  • Pirie BJS, George SG, Lytton D, Thomson JD (1984) Metal containing blood cells of oysters: ultrastructure histochemistry X-ray microanalysis. J Mar Biol Assoc UK 64:115–123

    Article  CAS  Google Scholar 

  • Roesijadi G, Brubacher LL, Unger ME, Anderson RS (1997) Metallothionein mRNA induction and generation of reactive oxygen species in molluscan hemocytes exposed to cadmium in vitro. Comp Biochem Physiol C 118:171–176

    Article  CAS  Google Scholar 

  • Sahaphong S, Linthong V, Wanichanon C, Riengrojpitak S, Kangwanrangsan N, Viyanant V, Upatham ES, Pumthong T, Chansue N, Sobhon P (2001) Morphofunctional study of the hemocytes of Haliotis asinina. J Shellfish Res 20:711–716

    Google Scholar 

  • Sauvé S, Hendawi M, Brousseau P, Fournier M (2002a) Phagocytic response of terrestrial and aquatic invertebrates following in vitro exposure to trace elements. Ecotoxicol Environ Saf 52:21–29

    Article  Google Scholar 

  • Sauvé S, Brousseau P, Pellerin J, Morin Y, Senécal L, Goudreau P, Fournier M (2002b) Phagocytic activity of marine and freshwater bivalves: in vitro exposure of hemocytes to metals (Ag, Cd, Hg and Zn). Aquat Toxicol 58:189–200

    Article  Google Scholar 

  • Serpentini A, Ghayor C, Hebert V, Galéra P, Pujol JP, Boucaud-Camou E, Lebel JM (2000) De novo synthesis and identification of collagen transcripts in hemocytes from the gastropod mollusc, Haliotis tuberculata. J Exp Zool 287:275–284

    Article  CAS  Google Scholar 

  • Soto M, Cajaraville MP, Marigomez I (1996) Tissue and cell distribution of copper, zinc and cadmium in the mussel, Mytilus galloprovincialis, determined by autometallography. Tissue Cell 28:557–568

    Article  CAS  Google Scholar 

  • Travers MA, Mirella Da Silva P, Le Goïc N, Marie D, Donval A, Huchette S, Koken M, Paillard C (2008a) Morphologic, cytometric and functional characterisation of abalone (Haliotis tuberculata) haemocytes. Fish Shellfish Immunol 24:400–411

    Article  CAS  Google Scholar 

  • Travers MA, Le Goïc N, Huchette S, Koken M, Paillard C (2008b) Summer immune depression associated with increased susceptibility of the European abalone, Haliotis tuberculata to Vibrio harveyi infection. Fish Shellfish Immunol 25:800–808

    Article  CAS  Google Scholar 

  • Voccia I, Krzystyniak K, Dunier M, Flipo D, Fournier M (1994) In vitro mercury-related cytotoxicity and functional impairment of the immune cells of rainbow trout (Oncorhyncus mykiss). Aquat Toxicol 29:27–48

    Article  Google Scholar 

  • Vouras C, Dailianis S (2012) Evidence for phosphatidylinositol-3-OH-kinase (PI3-kinase) involvement in Cd-mediated oxidative effects on hemocytes of mussels. Comp Biochem Physiol C 155:587–593

    CAS  Google Scholar 

  • Zhu X, Zhou J, Cai Z (2011) The toxicity and oxidative stress of TiO2, nanoparticles in marine abalone (Haliotis diversicolor supertexta). Mar Pollut Bull 63:334–338

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financed by GENERA-IRSES 247,559.

Author information

Authors and Affiliations

  1. Marine Ecotoxicology, UR 09-03, IPEIS BP 805, 3018, Sfax, Tunisia

    Rim Ladhar-Chaabouni, Monia Machreki-Ajmi & Amel Hamza-Chaffai

  2. Normandie Université, 14032, Caen, France

    Antoine Serpentini & Jean-Marc Lebel

  3. CNRS INEE, FRE 3,484 BioMEA, SFR ICORE, Université de Caen Basse-Normandie, Esplanade de la Paix, 14032, Caen, Cedex, France

    Antoine Serpentini & Jean-Marc Lebel

Authors
  1. Rim Ladhar-Chaabouni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monia Machreki-Ajmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antoine Serpentini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jean-Marc Lebel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Amel Hamza-Chaffai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rim Ladhar-Chaabouni.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ladhar-Chaabouni, R., Machreki-Ajmi, M., Serpentini, A. et al. Does a short-term exposure to cadmium chloride affects haemocyte parameters of the marine gastropod Haliotis tuberculata?. Environ Sci Pollut Res 22, 17343–17349 (2015). https://doi.org/10.1007/s11356-014-3387-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3387-5

Keywords

Search

Navigation