Effect of in vitro exposure to zinc on immunological parameters of haemocytes from the marine gastropod Haliotis tuberculata

Fish and Shellfish Immunology

Volumn 29, Issue 5, 2010, Pages 846-853

  Mottin, Elmina ^a,b   Caplat, Christelle ^b,c   Mahaut, Marie Laure ^d   Costil, Katherine ^a   Barillier, Daniel ^b   Lebel, Jean Marc ^a   Serpentini, Antoine ^a  

^a Biology and Innovative Therapeutics for Ovarian Cancers group   (France)

^b UNIVERSITÉ DE CAEN   (France)

^c CORRODYS ^*  (France)

^d CNAM Intechmer   (France)

Author keywords

Abalone; Haemocytes; Haliotis tuberculata; Immune parameters; Zinc

Indexed keywords

GASTROPODA; HALIOTIDAE; HALIOTIS TUBERCULATA; MOLLUSCA;

EID: 77956292317     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2010.07.022     Document Type: Article

References (66)

1. Zhou Q., Zhang J., Fu J., Shi, Jiang G. Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 2008, 606:135-150.
2. Eisler R. Zinc hazards to fish, wildlife and invertebrates: a synoptic review 1993, Biological report 10, US Department of interior, Fish and Wildlife Service, Washington, DC.
3. Sandstrom B. Bioavailability of zinc. Eur J Clin Nutr 1997, 51:17-19.
4. Chvapil M. New aspects in the biological role of zinc: a stabilizer of macromolecules and biological membranes. Life Sci 1973, 13:1041-1049.
5. Stohs S.J., Bagghi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 1995, 18:321-336.
6. Frassinetti S., Bronzetti G., Caltavuturo L., Cini M., Della Croce C. The role of zinc in life: a review. J Environ Pathol Toxicol Oncol 2006, 25:597-610.
7. Ibs K.-H., Rink L. Zinc-altered immune function. J Nutr 2003, 133:1452S-1456S.
8. Harris E.D. Biological monitoring of iron, zinc and copper. Biological monitoring of exposure to chemicals: metals 1991, 175-196. John Wiley and Sons, New York. H.K. Dillon, M.H. Ho (Eds.).
9. Dardenne M. Zinc and immune function. Eur J Clin Nutr 2002, 56:S20-S23.
10. Sahaphong S., Linthong V., Wanichanon C., Riengrojpitak S., Kangwanrangsan N., Viyanant V., et al. Morphofunctional study of the hemocytes of Haliotis asinina. J Shellfish Res 2001, 20:711-716.
11. Galloway T.S., Depledge M.H. Immunotoxicity in invertebrates: measurement and ecotoxicological relevance. Ecotoxicology 2001, 10:5-23.
12. Hooper C., Day R., Slocombe R., Handlinger J., Benkendorff K. Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish Shellfish Immunol 2007, 22:363-379.
13. Travers M.A., Mirella Da Silva P., Le Goïc N., Marie D., Donval A., Huchette S., et al. Morphologic, cytometric and functional characterisation of abalone (Haliotis tuberculata) haemocytes. Fish Shellfish Immunol 2008, 24:400-411.
14. Fagotti A., Di Rosa I., Simoncelli F., Pipe R.K., Panara F., Pascolini R. The effects of copper on actin and fibronectin organization in Mytilus galloprovinciallis haemocytes. Dev Comp Immunol 1996, 20:383-391.
15. Olabbarietta I., L'Azou B., Yuric S., Cambar J., Cajaraville M.P. In vitro effects of cadmium on two different animal cell models. Toxicol In Vitro 2001, 15:511-517.
16. Sauvé S., Brousseau P., Pellerin J., Morin Y., Senécal L., Goudreau P., et al. Phagocytic activity of marine and freshwater bivalves: in vitro exposure of hemocytes to metals (Ag, Cd, Hg and Zn). Aquat Toxicol 2002, 58:189-200.
17. Gagnaire B., Thomas-Guyon H., Renault T. In vitro effects of cadmium and mercury on pacific oyster, Crassostrea gigas (Thunberg), haemocytes. Fish Shellfish Immunol 2004, 16:501-512.
18. Duchemin M.B., Auffret M., Wessel N., Fortier M., Morin Y., Pellerin J., et al. 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 2008, 153:416-423.
19. Cheng W., Hsiao I.S., Hsu C.H., Chen J.C. Change in water temperature on the immune response of Taiwan abalone Haliotis diversicolor supersexta and its susceptibility to Vibrio parahaemolyticus. Fish Shellfish Immunol 2004, 17:235-243.
20. Cheng W., Juang F.M., Chen J.C. The immune response of Taiwan abalone Haliotis diversicolor supersexta and its susceptibility to Vibrio parahaemolyticus at different salinity levels. Fish Shellfish Immunol 2004, 16:295-306.
21. Travers M.A., Le Goïc N., Huchette S., Koken M., Paillard C. Summer immune depression associated with increased susceptibility of the European abalone Haliotis tuberculata to Vibrio harveyi infection. Fish Shellfish Immunol 2008, 25:800-808.
22. Wang S.H., Wang Y.L., Zhang Z.X., Ralph J., Weng Z.H., Zou Z.H., et al. Response of innate immune factors in abalone Haliotis diversicolor supersexta to pathogenic or non-pathogenic infection. J Shellfish Res 2004, 23:1173-1177.
23. Martello L.B., Friedman C.S., Tjeerdema R.S. Combined effects of pentachlorophenol and salinity stress on phagocytic and chemotactic function in two species of abalone. Aquat Toxicol 2000, 49:213-225.
24. Lebel J.-M., Giard W., Favrel P., Boucaud-Camou E. Effects of different vertebrate growth factors on primary cultures of hemocytes from the gastropod mollusc, Haliotis tuberculata. Biol Cell 1996, 86:67-72.
25. Poncet J.-M., Serpentini A., Thiébot B., Villers C., Bocquet J., Boucaud-Camou E., et al. 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 2000, 2:387-398.
26. Serpentini A., Ghayor C., Hebert V., Galéra P., Pujol J.-P., Boucaud-Camou E., et al. De novo synthesis and identification of collagen transcripts in hemocytes from the gastropod mollusc, Haliotis tuberculata. J Exp Zool 2000, 287:275-284.
27. Riinkevich B. Marine invertebrate cell cultures: new millennium trends. Mar Biotechnol 2005, 7:429-439.
28. Le Pennec G., Le Pennec M. Acinar primary cell culture from the digestive gland of Pecten maximus (L.): an original model for ecotoxcological purposes. J Exp Mar Biol Ecol 2001, 259:171-187.
29. Schirmer K. Proposal to improve vertebrate cell cultures to establish them as substitutes for the regulatory testing of chemicals and effluents using fish. Toxicology 2006, 224:163-183.
30. Wu J.P., Chen H.C., Huang D.J. Histopathological alterations in gills of white shrimp, Litopenaeus vannamei (Boone) after acute exposure to cadmium and zinc. Bull Environ Contam Toxicol 2009, 82:90-95.
31. Stabili L., Pagliara P. Effect of zinc on lusozyme-like activity of the seastar Marthasterias glacialis (Echinodermata Asteroidea) mucus. J Invertebr Pathol 2009, 100:189-192.
32. Farcy E., Serpentini A., Fiévet B., Lebel J.-M. Identification of cDNAs encoding HSP70 and HSP90 in the abalone Haliotis tuberculata: transcriptional induction in response to thermal stress in hemocyte primary culture. Comp Biochem Physiol B Biochem Mol Biol. 2007, 146:540-550.
33. Bachère E., Chagot D., Grizel H. Separation of Crassostrea gigas hemocytes by density gradient centrifugation and counterflow centrifugal elutriation. Dev Comp Immunol 1988, 12:549-559.
34. Gorski J., Nugegoda D. Toxicity of trace metals to juvenile abalone, Haliotis rubra following short-term exposure. Bull Environ Contam Toxicol 2006, 77:732-740.
35. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63.
36. Poncet J.-M., Serpentini A., Boucaud-Camou E., Lebel J.-M. Cryopreservation of mantle dissociated cells from Haliotis tuberculata (Gastropoda) and post-thawed primary cells cultures. Cryobiology 2002, 44:38-45.
37. Bass D.A., Parce J.W., Dechatelet L.R., Szejda P., Seeds M.C., Thomas M. Flow cytometric studies of oxidativeproduct formation by neutrophils: a graded response to membrane stimulation. J Immunol 1983, 130:1910-1917.
38. Lambert C., Soudant P., Choquet G., Paillard C. Measurement of Crassostrea gigas hemocyte oxidative metabolism by flow cytometry and the inhibiting capacity of pathogenic vibrios. Fish Shellfish Immunol 2003, 15:225-240.
39. Delaporte M., Soudant P., Moal J., Lambert C., Quere C., Miner P., et al. Effect of a mono-specific algal diet on immune functions in two bivalves species Crassostrea gigas and Ruditapes Philippinarum. J Exp Biol 2003, 206:3053-3064.
40. Hégaret H., Wikfors G.H., Soudant P. 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 2003, 293:249-265.
41. Labreuche Y., Soudant P., Gonçalves M., Lambert C., Nicolas J.L. Effect of extracellular products from the pathogenic Vibrio aestuarianus strain 01/32 on lethality and cellular immune responses of the oyster Crassostrea gigas. Dev Comp Immunol 2006, 30:367-379.
42. González F., Fárez-Vidal M.E., Arias J.M., Montoya E. Partial purification and biochemical properties of acid and alkaline phosphatases from Myxococcus coralloides D. J Appl Bacteriol 1994, 77:567-573.
43. Hernandez-Lopez J., Gollas-Galvan T., Gomez-Jimenez S., Portillo-Clark G., Vargas-Albores F. In the spiny lobster (Panulirus interruptus) the prophenoloxidase is located in plasma not in haemocytes. Fish Shellfish Immunol 2003, 14:105-114.
44. Bradford M.M. A refined and sensitive method for quantification of microgram quantities of proteins utilizing the principl of protein-dye binding. Anal Biochem 1976, 72:248-254.
45. Brousseau P., Pellerin J., Morin Y., Cyr D., Blakley B., Boermans H., et al. 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 2000, 142:145-156.
46. 2+-induced cell death is mediated by the induction of intracellular ROS in ARPE-19 cells. Curr Eye Res 2004, 28:195-201.
47. Gómez-Mendikute A., Cajaraville M.P. 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 2003, 17:539-546.
48. Larson K.G., Roberson B.S., Hetrick F.M. Effect of environmental pollutants on the chemiluminescence of hemocytes from the American oyster Crassostrea virginica. Dis Aquat Org 1989, 6:131-136.
49. Beckmann N., Morse M.P., Moore C.M. Comparative study of phagocytosis in normal and diseased hémocytes of the bivalve mollusc Mya arenaria. J Invertebr Pathol 1992, 59:124-132.
50. Cima F., Marin M.G., Matozzo V., Da Ros L., Ballarin L. Biomarkers for TBT immunotoxycity studies on the cultivated clam Tapes philippinarum (Adams and Reeve, 1850). Mar Pollut Bull 1999, 39:112-115.
51. Kaloyianni M., Ragia V., Tzeranaki I., Dailianis S. The influence of Zn on signaling pathways and attachment of Mytilus galloprovincialis haemocytes to extracellular matrix proteins. Comp Biochem Physiol C 2006, 144:93-100.
52. Thiagarajan R., Gopalakrishnan S., Thilagam H. Immunomodulation in the marine green mussel Perna viridis exposed to sub-lethal concentrations of Cu and Hg. Arch Environ Contam Toxicol 2006, 51:393-399.
53. Bado-Nilles A., Gagnaire B., Thomas-Guyon H., Le Floch S., Renault T. Effects of 16 pure hydrocarbons and two oils on haemocyte and haemolymphatic parameters in the Pacific oyster, Crassostrea gigas. Toxicol In Vitro 2008, 22:1610-1617.
54. Gagnaire B., Thomas-Guyon H., Burgeot Th, Renault T. Pollutant effects on Pacific oyster, Crassostrea gigas (Thunberg), hemocytes: screening of 23 molecules using flow cytometry. Cell Biol Toxicol 2006, 22:1-14.
55. Mazón L.I., Gonzalez G., Vicario A., Estomba A., Aguirre A. Inhibition of esterase in the marine gastropod Littorina littorea exposed to cadmium. Ecotoxicol Environ Saf 1998, 41:284-287.
56. Zvereva E., Serebrov V., Glupov V., Dubovskiy I. Activity and heavy metal resistance of non-specific esterase in leaf beetle Chrysomela lapponica from polluted and unpolluted habitats. Comp Biochem Physiol C 2003, 135:383-391.
57. Vallee B.L., Falchuk K.H. The biochemical basis of zinc physiology. Phys Rev 1993, 73:79-118.
58. Coles J.A., Pipe R.K. Phenoloxidase activity in the haemolymph and haemocytes of the marine mussel Mytilus edulis. Fish Shellfish Immunol 1994, 4:337-352.
59. Liu G., Yang L., Fan T., Cong R., Tang Z., Sun W., et al. Purification and characterization of phenoloxidase from crab Charybdis japonica. Fish Shellfish Immunol 2006, 20:47-57.
60. Lacoue-Labarthe T., Bustamante P., Hörlin E., Luna-Acosta A., Bado-Nilles A., Thomas-Guyon H. Phenoloxidase activation in the embryo of the common cuttlefish Sepia officinalis and responses to the Ag and Cu exposure. Fish Shellfish Immunol 2009, 27:516-521.
61. Tujula N., Radford J., Nair S.V., Raftos D.A. Effects of tributyltin and other metals on the phenoloxidase activating system of the tunicate, Styela plicata. Aquat Toxicol 2001, 55:191-201.
62. Mazorra M.T., Rubio J.A., Blasco J. Acid and alkaline phosphatase activities in the clam Scrobicularia plana: kinetic characteristics and effects of heavy metals. Comp Biochem Physiol B 2002, 131:241-249.
63. Jing G., Li Y., Xie L., Zhang R. Metal accumulation and enzyme activities in gills and digestive gland of pearl oyster (Pinctada fucata) exposed to copper. Comp Biochem Physiol C 2006, 144:184-190.
64. Rajalakshmi S., Mohandas A. Copper-induced changes in tissue enzyme activity in a freshwater mussel. Ecotoxicol Environ Saf 2005, 62:140-143.
65. Shuhong W., Yilei W., Zhaoxia Z., Jack R., Zhaohong W., Zhihua Z., et al. Response of innate immune factors in abalone Haliotis diversicolor supertexta to pathogenic or non-pathogenic infection. J Shellfish Res 2004, 23:1173-1177.
66. Nakayama K., Maruyama T. Differential production of active oxygen species in photo-symbiotic and non-symbiotic bivalves. Dev Comp Immunol 1998, 22:151-159.