Abstract
Among aquatic organisms suitable for biological monitoring, molluscs occupy a prominent place due to their wide geographic distribution, their abundance and accessibility in the field as well as in aquaculture. Molluscs reflect the degree of environmental contamination and are the most useful bioindicator tools. The study of modulation of immune system or immunomodulation in marine molluscs has become one of the privileged ways for evaluating the physiological effects of environmental factors. Physiological responses of molluscs to environmental stresses could be mediated by haemocytes. These cells are continually exposed to the external environment due to the open circulatory system of molluscs and are affected by pollutants. In fact, several studies showed the effects of different environmental contaminants on haemocyte functions (viability, phagocytosis, ROS production) as well as on proteins involved in cytoskeletal structure maintenance using the in vitro approaches. In ecotoxicology, in vitro approach is an alternative to animal testing due to the reduced use of experimental animals, low cost and rapid performance. Although several studies showed the importance of using in vitro cell models to determine the effects of different environmental contaminants on haemocyte parameters in marine molluscs, a few reviews highlight these effects. The main purpose of this paper is to summarize the recent data on the effect of some xenobiotics on haemocyte parameters in some mollusc species and then suggest future research prospects.
Similar content being viewed by others
References
Adema CM, Vanderknaap WPW, Sminia T (1991) Molluscan hemocyte-mediated cytotoxicity: the role of reactive oxygen intermediates. Rev Aquat Sci 4:201–223
Aladaileh S, Nair SV, Birch D, Raftos DA (2007) Sydney rock oyster (Saccostrea glomerata) hemocytes: morphology and function. J Invertebr Pathol 96:48–63
Anderson RS, Mora LM, Thomson SA (1994) Modulation of oyster (Crassostrea virginica) hemocyte immune function by copper, as measured by luminol-enhanced chemiluminiscence. Comp Biochem Physiol C 108:215–220
Armstrong DA, Armstrong JL, Krassner SM, Pauley GB (1971) Experimental wound repair in the black abalone Haliotis cracherodii. J Invertebr Pathol 17:216–227
Ashton-Alcox KA, Ford SE (1998) Variability in molluscan hemocytes: a flow cytometric study. Tissue Cell 30:195–204
Astuya A, Carrera C, Ulloa V, Aballay A, Núñez-Acuña G, Hégaret H, Gallardo-Escárate C (2015) Saxitoxin modulates immunological parameters and gene transcription in Mytilus chilensis hemocytes. Int J Mol Sci 16:15235–15250
Auffret M (1988) Bivalve hemocyte morphology. Am Fish Soc Spec Pub 18:169–177
Auffret M (1989) Comparative study of the hemocytes of two oyster species: the europeean flat oyster, Ostrea edulis (Linnaeus, 1750) and the pacific oyster, Crassostrea gigas (Thunberg, 1793). J Shellfish Res 8:367–373
Auzoux-Bordenave S, Domart-Coulon I (2010) Marine invertebrate cell culture as tools for biomineralization studies. J Sci Hal Aquat 2:42–47
Bado-Nilles A, Gagnaire B, Thomas-Guyon H, Le Floch S, Renault T (2008) Effects of 16 pure hydrocarbons and two oils on haemocyte and haemolymphatic parameters in the Pacific oyster, Crassostrea gigas (Thunberg). Toxicol Vitro 22:1610–1617
Ballarin L, Covre V, Masiero L, Casellato S (2014) Immunotoxic effects of fluoride on the hemocytes of Venerupis philippinarum. Invertebrate Surviv J 11:22–29
Barracco MA, Medeiros ID, Moreira FM (1999) Some haemato-immunological parameters in the mussel Perna perna. Fish Shellfish Immunol 9:387–404
Barth T, Moraes N, Barracco MA (2005) Evaluation of some hematoimmunological parameters in the mangrove oyster Crassostrea rhizophorae of different habitats of Santa Catarina Island, Brazil. Aquat Liv Res 18:179–186
Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313
Bernier J, Brousseau P, Krzystyniak K, Tryphonas H, Fournier M (1995) Great Lakes health effects: immunotoxicity of heavy metals. Environ Health Perspect 103:23–34
Bigas M, Durfort M, Poquet M (2006) Cytological response of hemocytes in the European flat oyster, Ostrea edulis, experimentally exposed to mercury. Biometals 19:659–673
Binelli A, Cogni D, Parolini M, Riva C, Provini A (2009) Cytotoxic and genotoxic effects of in vivo exposure to triclosan and trimethoprim on zebra mussel (Dreissena polymorpha) hemocytes. Comp Biochem Physiol C 150:50–56
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
Butler R, Roesijadi G (2000) Metallothionein (MT) gene expression and cadmium-induced immunotoxicity in haemocytes of the eastern oyster Crassostrea virginica. Mar Environ Res 50:465–472
Cajaraville MP, Pal SG (1995) Morphofunctional study of the hemocytes of the bivalve mollusc Mytilus galloprovincialis with emphasis on the endolysosomal compartment. Cell Struct Funct 20:355–367
Canesi L, Ciacci C, Lorusso LC, Betti M, Gallo G, Pojana G, Marcomini A (2007a) Effects of triclosan on Mytilus galloprovincialis hemocyte function and digestive gland enzyme activities: possible modes of action on non target organisms. Comp Biochem Physiol C Toxicol Pharmacol 145:464–472
Canesi L, Lorusso L, Ciacci C, Betti M, Rochi M, Pojana G, Marcomini A (2007b) Immunomodulation of Mytilus hemocytes by individual estrogenic chemicals and environmentally relevant mixtures of estrogens: in vitro and in vivo studies. Aquat Toxiol 81:36–44
Carballal MJ, Lopez C, Azevedo C, Villalba A (1997) Hemolymph cell types of the mussel Mytilus galloprovincialis. Dis Aquat Org 29:127–135
Chang SJ, Tseng SM, Chou HY (2005) Morphological characterization via light and electron microscopy of the hemocytes of two cultures bivalves: a comparison study between the hard clam (Meretrix lusoria) and Pacific oyster (Crassostrea gigas). Zool Stud 44:144–153
Chen JH, Yang HY, Peng SW, Chen YJ, Tsai KY (1996) Characterisation of abalone (Haliotis diversicolor) hemocytes in vitro. Biol Bull 31:31–38
Cheng TC (1981) Bivalves. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells. Academic Press, London, pp 233–300
Cheng TC (1996) Hemocytes: forms and functions. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern Oyster Crassostrea virginica. Maryland Sea Grant Book, College Park, pp 299–333
Cheng TC, Sullivan JT (1984) Effects of heavy metals on phagocytosis by mollusca hemocytes. Mar Environ Res 14:305–315
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
Ciacci C, Barmo C, Fabbri R, Canonico B, Gallo G, Canesi L (2011) Immunomodulation in Mytilus galloprovincialis by non-toxic doses of hexavalent chromium. Fish Shellfish Immunol 31:1026–1033
Ciacci C, Canonico B, Bilanicova D, Fabbri R, Cortese K, Gallo G, Marcomini A, Pojana G, Canesi L (2012) Immunomodulation by different types of n-oxides in the hemocytes of the marine bivalve Mytilus galloprovincialis. PLoS ONE 7:e36937
Cima F, Matozzo V, Marin MG, Ballarin L (2000) Haemocytes of the clam Tapes philippinarum (Adams & Reeve, 1850): morphofunctional characterisation. Fish Shellfish Immunol 10:677–693
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
De Guise S, Bernier J, Martineau D, Béland P, Fournier M (1997) In vitro exposure of beluga whale lymphocytes to selected heavy metals. Environ Toxicol Chem 15:1357–1364
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
Domart-Coulon I, Doumenc D, Auzoux-Bordenave S, Fichant YL (1994) Identification of media supplements that improve the viability of primarily cell cultures of Crassostrea gigas oysters. Cytotechnology 16:109–120
Domart-Coulon I, Auzoux-Bordenave S, Doumenc D, Khalanski M (2000) Cytotoxicity assessment of antibiofouling compounds and by-products in marine bivalve cell cultures. Toxicol In Vitro 14:245–251
Donaghy L, Kim BK, Hong HK, Park HS, Choi KS (2009) Flow cytometry studies on the populations and immune parameters of the hemocytes of the Suminoe oyster, Crassostrea ariakensis. Fish Shellfish Immunol 27:296–301
Donaghy L, Hong HK, Lambert C, Park HS, Shim WJ, Choi KS (2010) First characterisation of the populations and immune-related activities of hemocytesfrom two edible gastropod species, the disk abalone, Haliotis discus discus and the spiny top shell, Turbo cornutus. Fish Shellfish Immunol 28:87–97
Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95
Duchemin MB, Fournier M, Auffret M (2007) Seasonal variations of immune parameters in diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg). Aquaculture 264:73–81
Duchemin M, Auffret M, Wessel N, Fortier M, Morin Y, Pellerin J, Fournier M (2008) Multiple experimental approaches of immunotoxic effects of mercury chloride in the blue mussel, Mytilus edulis, through in vivo, in tubo and in vitro exposures. Environ Pollut 153:416–423
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
Foley DA, Cheng TC (1974) Morphology, hematologic parameters, and behavior of hemolymph cells of the quahaug clam, Mercenaria mercenaria. Biol Bull 146:343–356
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
Fugere N, Brousseau P, Krzystyniak K, Coderre D, Fournier M (1996) Heavy metal-specific inhibition of phagocytosis and different in vitro sensitivity of heterogeneous coelomocytes from Lumbricus terrestris (Oligochaeta). Toxicology 109:157–166
Gagnaire B, Renault T, Bouilly K, Lapegue S, Thomas-Guyon H (2003) Study of atrazine effects on Pacific oyster, Crassostrea gigas, haemocytes. Curr Pharm Des 9:193–199
Gagnaire B, Thomas-Guyon H, Renault T (2004) In vitro effects of cadmium and mercury on Pacific oyster, Crassostrea gigas (Thunberg), haemocytes. Fish Shellfish Immunol 16:501–512
Gagnaire B, Thomas-Guyon H, Burgeot Th, Renault T (2006) Pollutant effects on Pacific oyster, Crassostrea gigas (Thunberg), hemocytes: screening of 23 molecules using flow cytometry. Cell Biol Toxicol 22:1–14
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 C Toxicol Pharmacol 156:87–94
Girón-Pérez MI (2010) Relationships between innate immunity in bivalve molluscs and environmental pollution. Invertebrate Surviv J 7:149–156
Goedken M, DeGuise S (2004) Flow cytometry as a tool to quantify oyster defense mechanisms. Fish Shellfish Immunol 16:539–552
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
Gopalakrishnan S, Thilagam H, Huang WB, Wang KJ (2009) Immunomodulation in the marine gastropod Haliotis diversicolor exposed to benzo(a)pyrene. Chemosphere 75:389–397
Gorbushin AM, Iakovleva NV (2006) Haemogram of Littorina littorea. J Mar Biol Assoc UK 86:1175–1181
Halm-Lemeille MP, Abbaszadeh Fard E, Latire T, Ferard JF, Costil K, Lebel JM, Bureau R, Serpentini A (2014) The effect of different polychlorinated biphenyls on two aquatic models, the green alga Pseudokirchneriella subcapitata and the haemocytes from the European abalone Haliotis tuberculata. Chemosphere 110:120–128
Hègaret H, Wikfors GH, Soudant P (2003) Flow-cytometric analysis of haemocytes from eastern oysters, Crassostrea virginica, subjected to a sudden temperature elevation; I. Haemocyte types and morphology. J Exp Mar Biol Ecol 293:237–248
Hine PM (1999) The inter-relationships of bivalve haemocytes. Fish Shellfish Immunol 9:367–385
Höher N, Köhler A, Strand J, Broeg K (2012) Effects of various pollutant mixtures on immune responses of the blue mussel (Mytilus edulis) collected at a salinity gradient in Danish coastal waters. Mar Environ Res 75:35–44
Huffman JE, Tripp MR (1982) Cell types and hydrolytic enzymes of soft shell clam (Mya arenaria) hemocytes. J Invertebr Pathol 40:68–74
Hurtado MA, Da Silva PM, Le Goïc N, Palacios E, Soudant P (2011) Effect of acclimatization on hemocyte functional characteristics of the Pacific oyster (Crassostrea gigas) and carpet shell clam (Ruditapes decussatus). Fish Shellfish Immunol 31:978–984
Kaloyianni M, Ragia V, Tzeranaki I, Dailianis S (2006) The influence of Zn on signalling pathways and attachment of Mytilus galloprovincialis haemocytes to extracellular matrix proteins. Comp Biochem Physiol C Toxicol Pharmacol 144:93–100
Katsumiti A, Gilliland D, Arostegui I, Cajaraville MP (2014) Cytotoxicity and cellular mechanisms involved in the toxicity of CdS quantum dots in hemocytes and gill cells of the mussel Mytilus galloprovincialis. Aquat Toxicol 53:39–52
Katsumiti A, Arostegui I, Oron M, Gilliland D, Valsami-Jones E, Cajaraville MP (2015) Cytotoxicity of Au, ZnO and SiO2 NPs using in vitro assays with mussel hemocytes and gill cells: relevance of size, shape and additives. Nanotoxicology 12:1–9
Kehrer JP (1993) Free radicals as mediators of tissue injury and disease. Crit Rev Toxicol 23:21–48
Krzystyniak K, Flipo D, Mansour S, Fournier M (1989) Suppression of avidin processing and presentation by mouse macrophages after sublethal exposure to dieldrin. Immunopharmacology 18:157–166
Labreuche Y, Soudant P, Goncalves M, Lambert C, Nicolas JL (2006) Effects of extracellular products from pathogenic Vibrio aestuarianus strain 01/32 on lethality and cellular immune responses of the oyster Crassostrea gigas. Dev Comp Immunol 30:367–379
Ladhar-Chaabouni R, Machreki-Ajmi M, Serpentini A, Lebel JM, Hamza-Chaffai A (2014) Does a short term exposure to cadmium chloride affects haemocyte parameters of the marine gastropod Haliotis tuberculata? Environ Sci Pollut Res 22:17343–17349
Lambert C, Soudant P, Choquet G, Paillard C (2003) Measurement of Crassostrea gigas haemocyte oxidative metabolism by flow cytometry and the inhibiting capacity of pathogenic vibrios. Fish Shellfish Immunol 15:225–240
Lambert C, Soudant P, Jegaden M, Labreuche Y, Rifi M, Moal J (2005) Modulation of Reactive Oxygen Species (ROS) production by hemocyte of two aquacultured bivalves, clam and oyster, faced to pathogenic vibrio. In: Moal J, Soudant P, Volety AK (eds) Book of abstract: 8th international conference on shellfish restoration, Brest, France, p. 60 abstract only
Lambert C, Soudant P, Jegaden M, Delaporte M, Labreuche Y, Moal J, Samain JF (2007) In vitro modulation of reactive oxygen and nitrogen intermediate (ROI/RNI) production in Crassostrea gigas hemocytes. Aquaculture 270:413–421
Langston WJ, Bebianno MJ (eds) (1998) Metal metabolism in aquatic environments. Chapman and Hall, London, p 488
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
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
Li H, Hu J, Xin W, Zhao B (2000) Production and interaction of oxygen and nitric oxide free radicals in PMA stimulated macrophages during the respiratory burst. Redox Rep 5:353–358
Livingstone DR, Garcia-Martinez P, Michel X, Narbonne JF, O’Hara S, Ribera D, Winston GW (1990) Oxyradical production as a pollution-mediated mechanism of toxicity in the common mussel, Mytilus edulis and other molluscs. Funct Ecol 4:415–424
López C, Carballal MJ, Azevedo C, Villalba A (1997a) Morphological characterization of the hemocytes of the clam, Ruditapes decussatus (Mollusca: Bivalvia). J Invertebr Pathol 69:51–57
López C, Carballal MJ, Azevedo C, Villalba A (1997b) Enzyme characterisation of the circulating hemocytes of the carpet shell clam Ruditapes decussatus (Mollusca: Bivalvia). Fish Shellfish Immunol 7:595–608
López C, Carballal MJ, Azevedo C, Villalba A (1997c) Differential phagocytic ability of the circulating haemocyte types of the carpet shell clam Ruditapes decussatus (Mollusca: Bivalvia). Dis Aquat Org 30:209–215
Marisa I, Marin MG, Caicci F, Franceschinis E, Martucci A, Matozzo V (2015) In vitro exposure of haemocytes of the clam Ruditapes philippinarum to titanium dioxide (TiO2) nanoparticles: nanoparticle characterisation, effects on phagocytic activity and internalisation of nanoparticles into haemocytes. Mar Environ Res 103:11–17
Martin GG, Oakes CT, Tousignant HR, Crabtree H, Yamakawa R (2007) Structure and function of haemocytes in two marine gastropods, Megathura crenulata and Aplysia californica. J Mollus Stud 73:355–365
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, Marin MG (2010) First evidence of gender-related differences in immune parameters of the clam Ruditapes philippinarum (Mollusca: Bivalvia). Marine Biol 157:1181–1189
Matozzo V, Costa Devoti A, Marin M (2011) Immunotoxic effects of triclosan in the clam Ruditapes philippinarum. Ecotoxicology 21:66–74
Minguez L, Halm-Lemeille MP, Costil K, Bureau R, Lebel JM, Serpentini A (2014) Assessment of cytotoxic and immunomodulatory properties of four antidepressants on primary cultures of abalone hemocytes (Haliotis tuberculata). Aquat Toxicol 153:3–11
Moore CA, Eble EF (1977) Cytochemical aspects of Mercenaria mercenaria hemocytes. Biol Bull 152:105–119
Moreau P, Burgeot T, Renault T (2014) Pacific oyster (Crassostrea gigas) hemocyte are not affected by a mixture of pesticides in short-term in vitro assays. Environ Sci Pollut Res 21:4940–4949
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
Mount AS, Wheeler AP, Paradkar RP, Snider D (2004) Hemocyte-mediated shell mineralization in the eastern oyster. Science 304:297–300
Nakahara H, Bevelander G (1969) An electron microscope study of ingestion of thorotrast by amoebocytes of Pinctada radiata. Tex Rep Biol Med 27:101–109
Nzengue Y, Steiman R, Garrel C, Lefèvre E, Guiraud P (2008) Oxidative stress and DNA damage induced by cadmium in the human keratinocyte HaCat cell line: role of glutathione in the resistance to cadmium. Toxicology 243:193–206
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
Oubella R, Maes P, Allam B, Paillard C, Auffret M (1996) Selective induction of hemocytic response in Ruditapes philippinarum (Bivalvia) by different species of Vibrio (Bacteria). Aquat Liv Res 9:137–143
Parolini M, Quinn B, Binelli A, Provini A (2011) Cytotoxicity assessment of four pharmaceutical compounds on the zebra mussel (Dreissena polymorpha) haemocytes, gill and digestive gland primary cell cultures. Chemosphere 84:91–100
Pipe RK (1990) Hydrolytic enzymes associated with the granular haemocytes of the marine mussel Mytilus edulis. Histochem J 22:595–603
Pipe RK (1992) Generation of reactive oxygen metabolites by the haemocytes of the mussel Mytilus edulis. Dev Comp Immunol 16:111–122
Pipe RK, Farley SR, Coles JA (1997) The separation and characterization of haemocytes from the mussel Mytilus edulis. Cell Tissue Res 289:537–545
Pollero RJ, Huca G, Brenuer RR (1985) Role of hemocytes and plasma on lipid transport in freshwater mollusk Diplodon delodontus. Comp Biochem Physiol A Physiol 82:339–343
Poncet JM, Serpentini A, Thiébot B, Villers C, Bocquet J, Boucaud-Camou E, Lebel JM (2000) In vitro synthesis of proteoglycans and collagen in primary cultures of mantle cells from the nacreous mollusk, Haliotis tuberculata: a new model for study of molluscan extracellular matrix. Mar Biotechnol 2:387–398
Rifi M (2005) Etude de la production d’Espèces Oxygénées Réactives (EOR) par les hémocytes de la palourde japonaise Ruditapes philippinarum. Master of Science Thesis, University of Bretagne Occidentale, Brest, France (in French)
Riinkevich B (2005) Marine invertebrate cell cultures: new millennium trends. Mar Biotechnol 7:429–439
Rioult D, Lebel J-M, Le-Foll F (2013) Cell tracking and velocimetric parameters analysis as an approach to assess activity of mussel (Mytilus edulis) hemocytes in vitro. Cytotechnology 65:749–758
Roesijadi G, Brubacher LL, Unger ME, Anderson RS (1997) MetallothioneinmRNAinduction and generation of reactive oxygen species inmolluscan hemocytes exposed to cadmium in vitro. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 118:171–176
Sahaphong S, Linthong V, Wanichanon C, Riengrojpitak S, Kangwanrangsan N, Viyanant V et al (2001) Morphofunctional study of the hemocytes of Haliotis asinina. J Shellfish Res 20:711–716
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
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
Segal A (2008) The function of the NADPH oxidase of phagocytes and its relationship to other NOXs in plants, invertebrates, and mammals. Int J Biochem Cell Biol 40:604–618
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
Terahara K, Takahashi KG, Nakamura A, Osada M, Yoda M, Hiroi T, Hirasawa M, Mori K (2006) Differences in integrin-dependent phagocytosis among three hemocyte subpopulations of the Pacific oyster Crassostrea gigas. Dev Comp Immunol 30:667–683
Thiagarajan R, Gopalakrishnan S, Thilagam H (2006) Immunomodulation in the marine green mussel Perna viridis exposed to sub-lethal concentrations of Cu and Hg. Arch Environ Contam Toxicol 51:393–399
Toreilles J, Guérin MC, Roch P (1996) Reactive oxygen species and defense mechanisms in marine bivalves. C R Acad Sci Ser III 319:209–218 (in French)
Travers MA, Mirella Da Silva P, Le Goïc N, Marie D, Donval A, Huchette S, Koken M, Paillard C (2008a) Morphologic, cytometric and functional characterization of abalone (Haliotis tuberculata) haemocytes. Fish Shellfish Immunol 24:400–411
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
Tripp MR (1961) The fate of foreign materials experimentally introduced into the snail Australorbis glabratus. J Parasitol 47:745–751
Van der Merwe M, Auzoux-Bordenave S, Niesler C, Roodt-Wilding R (2010) Investigating the establishment of primary cell culture from different abalone (Haliotis midae) tissues. Cytotechnology 62:265–277
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
Vouras C, Dailianis S (2012) Evidence for phosphatidylinositol-3-OHkinase (PI3-kinase) involvement in Cd-mediated oxidative effects on hemocytes of mussels. Comp Biochem Physiol C Toxicol Pharmacol 155:587–593
Winston GW, Moore MN, Kirchin MA, Soverchia C (1996) Production of reactive oxygen species by hemocytes from the marine mussel, Mytilus edulis: lysosomal localization and effect of xenobiotics. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 113:221–229
Wong S, Fournier M, Coderre D, Banska W, Krzystyniak K (1992) Environmental immunotoxicology. In: Peakall D (ed) Animal biomarkers as pollution indicators. Chapman and Hall/CRC Press, Boca Raton, pp 167–189
Xue QG, Renault T, Chilmonczyk S (2001) Flow cytometric assessment of haemocyte sub-populations in the European flat oyster, Ostrea edulis, haemolymph. Fish Shellfish Immunol 11:557–567
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ladhar-Chaabouni, R., Hamza-Chaffai, A. The cell cultures and the use of haemocytes from marine molluscs for ecotoxicology assessment. Cytotechnology 68, 1669–1685 (2016). https://doi.org/10.1007/s10616-015-9932-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10616-015-9932-3