First characterisation of the populations and immune-related activities of hemocytes from two edible gastropod species, the disk abalone, Haliotis discus discus and the spiny top shell, Turbo cornutus

Fish and Shellfish Immunology

Volumn 28, Issue 1, 2010, Pages 87-97

  Donaghy, Ludovic ^a,b   Hong, Hyun Ki ^a   Lambert, Christophe ^b   Park, Heung Sik ^c   Shim, Won Joon ^c   Choi, Kwang Sik ^a  

^a Jeju National University   (South Korea)

^b Universite de Bretagne Occidentale   (France)

^c Korea Research Institute of Ships and Ocean Engineering   (South Korea)

Author keywords

Disk abalone; Flow cytometry; Hemocytes; Lysosomes; Oxidative activity; Phagocytosis; Spiny top shell

Indexed keywords

BATILLUS CORNUTUS; GASTROPODA; HALIOTIDAE; HALIOTIS DISCUS DISCUS; TROCHIDAE;

EID: 73249143651     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2009.10.006     Document Type: Article

References (107)

1. Cheng T.C. Functional morphology and biochemistry of molluscan phagocytes. Ann NY Acad Sci 266 (1975) 343-379
2. Cheng T.C. Bivalves. In: Ratcliffe N.A., and Rowly A.F. (Eds). Invertebrate blood cells (1981), Academic Press, London, UK 233-300
3. Sminia T. Gastropods. In: Ratcliffe N.A., and Rowly A.F. (Eds). Invertebrate blood cells (1981), Academic Press, London, UK 191-232
4. Pollero R.J., Huca G., and Brenuer R.R. Role of hemocytes and plasma on lipid transport in freshwater mollusk. Diplodon delodontus. Comp Biochem Physiol 82A (1985) 339-343
5. Cheng T.C. Hemocytes: forms and functions. In: Kennedy V.S., Newell R.I.E., and Eble A.F. (Eds). The eastern oyster Crassostrea virginica (1996), Maryland Sea Grant Book, College Park, MD, USA 299-333
6. Beninger P.G., Le Pennec G., and Le Pennec M. Demonstration of nutrient pathway from the digestive system to oocytes in the gonad intestinal loop of the scallop Pecten maximus L. Biol Bull 205 (2003) 83-92
7. Armstrong D.A., Armstrong J.L., Krassner S.M., and Pauley G.B. Experimental wound repair in the black abalone. Haliotis cracherodii. J Invertebr Pathol 17 (1971) 216-227
8. Sparks A.K., and Morado J.F. Inflammation and wound repair in bivalve molluscs. In: Fisher W.S. (Ed). Disease processes in marine bivalve molluscs vol. 18 (1988), American Fisheries Society, Bethesda, MD, USA 139-152
9. Mount A.S., Wheeler A.P., Paradkar R.P., and Snider D. Hemocyte-mediated shell mineralization in the eastern oyster. Science 304 (2004) 297-300
10. Matozzo V., Ballarin L., Pampanin D.M., and Marin M.G. Effects of copper and cadmium exposure on functional responses of hemocytes in the clam, Tapes philippinarum. Arch Environ Contam Toxicol 41 (2001) 163-170
11. Fisher W.S. Antimicrobial activity of copper and zinc accumulated in eastern oyster amebocytes. J Shellfish Res 23 (2004) 321-351
12. Fisher W.S. Relationship of amebocytes and terrestrial elements to adult shell deposition in eastern oysters. J Shellfish Res 23 (2004) 353-367
13. Tripp M.R. The fate of foreign materials experimentally introduced into the snail Australorbis glabratus. J Parasitol 47 (1961) 745-751
14. Bayne C.J. Molluscan internal defence mechanism: the fate of C14 labelled bacteria in the land snail Helix pomatia (L.). J Comp Physiol 86 (1973) 17-25
15. Van der Knaap W.P.W., Sminia T., Kroese F.G.M., and Dikkeboom R. Elimination of bacteria from the circulation of the pond snail Lymnaea stagnalis. Dev Comp Immunol 5 (1981) 21-32
16. Cheng T.C. Cellular defense mechanisms in oysters. In: Fingerman N., and Nagabhushanam R. (Eds). Recent advances in marine biotechnology. Immuno-biology and pathology (2000), Science Publishers, Enfield, NH, USA 43-83
17. Chu F.L.E. Defense mechanisms of marine bivalves. In: Fingerman N., and Nagabhushanam R. (Eds). Recent advances in marine biotechnology. Immuno-biology and pathology (2000), Science Publishers, Enfield, NH, USA 1-42
18. Canesi L., Gallo G., Gavioloi M., and Pruzzo C. Bacteria-hemocyte interactions and phagocytosis in marine bivalves. Microsc Res Tech 57 (2002) 469-476
19. Harris K.R. The fine structure of encapsulation in Biomphalaria glabrata. Ann NY Acad Sci 266 (1975) 446-463
20. Krupa P.L., Lewis L.M., and Vecchio P.D. Schistosoma haematobium in Bulinus guernei: electron microscopy of hemocyte-sporocyst Interactions. J Invert Pathol 30 (1977) 35-45
21. Chagot D., Comps M., Boulo V., Ruano F., and Grizel H. Histological study of a cellular reaction in Ruditapes decussatus infected by a protozoan. Aquaculture 67 (1987) 260-261
22. Montes J.F., Mercè D., and Garcia-Valero J. Cellular defense mechanism of the clam Tapes semidecussatus against infection by the protozoan Perkinsus sp. Cell Tissue Res 279 (1995) 529-538
23. Chu F.L.E. Humoral defense factors in marine bivalves. Am Fish Soc Spec Publ 18 (1988) 178-188
24. Hine P.M. The inter-relationships of bivalve haemocytes. Fish Shellfish Immunol 9 (1999) 367-385
25. Gosling E. Bivalve molluscs. Biology, ecology and culture (2002), Blackwell Publishing, Oxford, UK
26. Yoshino T.P., and Granath Jr. W.O. Identification of antigenically distinct hemocyte subpopulations in Biomphalaria glabrata (Gastropoda) using monoclonal antibodies to surface membrane markers. Cell Tissue Res 232 (1983) 553-564
27. Matricon-Gondran M., and Letocart M. Internal defenses of the snail Biomphalaria glabrata: I. Characterization of hemocytes and fixed phagocytes. J Invertebr Pathol 74 (1999) 224-234
28. Matricon-Gondran M., and Letocart M. Internal defenses of the snail Biomphalaria glabrata. II. In vivo responses of hemocytes and fixed phagocytes to injected foreign materials. J Invertebr Pathol 74 (1999) 235-247
29. Hahn U.K., Bender R.C., and Bayne C.J. Production of reactive oxygen species by hemocytes of Biomphalaria glabrata: carbohydrate-specific stimulation. Dev Comp Immunol 24 (2000) 531-541
30. 2 than susceptible snails. J Parasitol 91 (2005) 275-279
31. Humphries J.E., and Yoshino T.P. Regulation of hydrogen peroxide release in circulating hemocytes of the planorbid snail Biomphalaria glabrata. Dev Comp Immunol 32 (2008) 554-562
32. Dikkeboom R., van der Knapp W.P.W., Maaskant J.J., and de Jonge A.J.R. Different subpopulations of haemocytes in juvenile, adult and Trichobilharzia infected Lymnaea stagnalis: a characterisation using monoclonal antibodies. Z Parasitenkd Parasitol Res 71 (1985) 815-819
33. 2 production by hemocytes of the trematode intermediate host Lymnaea stagnalis (Gastropoda). Dev Comp Immunol 29 (2005) 305-314
34. 2 production and downstream ERK activation. J Exp Biol 209 (2006) 4829-4840
35. Wright B., Lacchini A.H., Davies A.J., and Walker A.J. Regulation of nitric oxide production in Lymnaea stagnalis defence cells: a role for protein kinase C and extracellular signal-regulated kinase signalling pathways. Biol Cell 98 (2006) 265-278
36. Russo J., and Madec L. Haemocyte apoptosis as a general cellular immune response of Lymnaea stagnalis (Gastropoda, Pulmonata) to a toxican. Cell Tissue Res 328 (2007) 431-441
37. Russo J., Madec L., and Brehélin M. Effect of a toxicant on phagocytosis pathways in the freshwater snail Lymnaea stagnalis. Cell Tissue Res 333 (2008) 147-158
38. Bayne C.J. Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Mol Biochem Parasitol 165 (2009) 8-18
39. Odom R., James W., and Berger T. Andrews' diseases of the skin: clinical dermatology. 9th ed. (2000), WB Saunders Company, Philadelphia
40. Chen J.H., Yang H.Y., Peng S.W., Chen Y.J., and Tsai K.Y. Characterization of abalone (Haliotis diversicolor) hemocytes in vitro. Biol Bull 31 (1996) 31-38
41. Gopalakrishnan S., Thilagam H., Huang W.B., and Wang K.J. Immunomodulation in the marine gastropod Haliotis diversicolor exposed to benzo(a)pyrene. Chemosphere 75 (2009) 389-397
42. 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 20 (2001) 711-716
43. Martello L.B., Friedman C.S., and Tjeedema R.S. Combined effects of pentachlorophenol and salinity stress on phagocytic and chemotactic function in two species of abalone. Aquat Toxicol 49 (2000) 213-225
44. Martello L.B., and Tjeerdema R.S. Combined effects of pentachorophenol and salinity stress on chemiluminescence activity in two species of abalone. Aquat Toxicol 51 (2001) 351-362
45. Malham S.K., Lacoste A., Gélébart F., Cueff A., and Poulet S.A. Evidence for a direct link between stress and immunity in the mollusk. Haliotis tuberculata. J Exp Zool 295A (2003) 136-144
46. Travers M.A., da Silva M.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 24 (2008) 400-411
47. Travers M.A., Le Goïc N., Huchette S., Koken M., and Paillard C. Summer immune depression associated with increased susceptibility of the European abalone, Haliotis tuberculata to Vibrio harveyi infection. Fish Shellfish Immunol 25 (2008) 800-808
48. Adamowicz A., and Bolaczek M. Blood cells morphology of the snail Helix aspersa maxima (Helicidae). Zool Pol 48 (2003) 93-101
49. Gorbushin A.M., and Iakovleva N.V. Haemogram of Littorina littorea. J Mar Biol Assoc UK 86 (2006) 1175-1181
50. Martin G.G., Oakes C.T., Tousignant H.R., Crabtree H., and Yamakawa R. Structure and function of haemocytes in two marine gastropods, Megathura crenulata and Aplysia californica. J Mollus Stud 73 (2007) 355-365
51. Mahilini H.M., and Rajendran A. Categorization of hemocytes of three gastropod species Trachea vittata (Muller), Pila globosa (Swainson) and Indoplanorbis exustus (Dehays). J Invertebr Pathol 97 (2008) 20-26
52. Adema C.M., Harris R.A., and van Deutekom-Mulder E.C. A comparative study of hemocytes from six different snails: morphology and functional aspects. J Invertebr Pathol 59 (1992) 24-32
53. Ford S.E., Ashton-Alcox K.A., and Kanaley S.A. Comparative cytometric and microscopic analyses of oyster haemocytes. J Invertebr Pathol 64 (1994) 114-122
54. Ashton-Alcox K.A., and Ford S.E. Variability in molluscan hemocytes: a flow cytometric study. Tissue Cell 30 (1998) 195-204
55. Renault T., Xue Q.G., and Chilmonczyk S. Flow cytometric analysis of European flat oyster, Ostrea edulis, haemocytes using a monoclonal antibody specific for granulocytes. Fish Shellfish Immunol 11 (2001) 269-274
56. Xue Q.G., Renault T., and Chilmonczyk S. Flow cytometric assessment of haemocyte sub-populations in the European flat oyster, Ostrea edulis, haemolymph. Fish Shellfish Immunol 11 (2001) 557-567
57. Delaporte M., Soudant P., Moal J., Lambert C., Quéré C., Miner P., et al. Effect of mono-specific algal diet on immune functions in two bivalve species - Crassostrea gigas and Ruditapes philippinarum. J Exp Biol 206 (2003) 3053-3064
58. Hégaret H., Wikfors G.H., and Soudant P. 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 (2003) 237-248
59. Hégaret H., Wikfors G.H., and 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 293 (2003) 249-265
60. Goedken M., and DeGuise S. Flow cytometry as a tool to quantify oyster defense mechanisms. Fish Shellfish Immunol 16 (2004) 539-552
61. Donaghy L., Kim B.K., Hong H.K., Park H.S., and Choi K.S. Flow cytometry studies on the populations and immune parameters of the hemocytes of the Suminoe oyster, Crassostrea ariakensis. Fish Shellfish Immunol 27 (2009) 296-301
62. Russo J., and Lagadic L. Effects of environmental concentrations of atrazine on hemocyte density and phagocytic activity in the pond snail Lymnaea stagnalis (Gastropoda, Pulmonata). Environ Poll 127 (2004) 303-311
63. Cossarizza A., Pinti M., Troiano L., and Cooper E. Flow cytometry as a tool for analyzing invertebrate cells. Invertebr Surv J 2 (2005) 32-40
64. Auffret M. Bivalve hemocyte morphology. Am Fish Soc Spec Publ 18 (1988) 169-177
65. Barraco M.A., Steil A.A., and Gargioni R. Morphological characterization of the hemocytes of the pulmonate snail Biomphalaria tenagophila. Mem Inst Osw Cruz 88 (1993) 73-83
66. Cima F., Matozzo V., Marin M.G., and Ballarin L. Haemocytes of the clam Tapes philippinarum (Adams & Reeve, 1850): morphofunctional characterisation. Fish Shellfish Immunol 10 (2000) 677-693
67. Aladaileh S., Nair S.V., Birch D., and Raftos D.A. Sydney rock oyster (Saccostrea glomerata) hemocytes: morphology and function. J Invertebr Pathol 96 (2007) 48-63
68. Hayakawa J., Yamakawa T., and Aoki I. Long-term fluctuation in the abundance of abalone and top shell in Japan and factors affecting those fluctuations. Bull Jpn Soc Fish Oceanogr 71 (2007) 96-105 [in Japanese with English abstract]
69. Auffret M., and Oubella R. Cytological and cytometric analysis of bivalves mollusc hemocytes. In: Stolen J.S., Fletcher T.C., Smith S.A., Zelikoff J.T., Kaattari S.L., Anderson R.S., Söderhäll K., and Weeks-Perkins B.A. (Eds). Techniques in fish immunology (1995), SOS Publications, Fair Haven 55-64
70. Rao K.M., Padmanabhan J., Kilby D.L., Cohen H.J., Currie M.S., and Weinberg J.B. Flow cytometric analysis of nitric oxide production in human neutrophils using dichlorofluorescein diacetate in the presence of a calmodulin inhibitor. J Leukoc Biol 51 (1992) 496-500
71. Curtin J.F., Donovan M., and Cotter T.G. Regulation and measurement of oxidative stress in apoptosis. J Immunol Methods 265 (2002) 49-72
72. Wardman P. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic Biol Med 43 (2007) 995-1022
73. Gomes A., Fernandes E., and Lima J. Fluorescence probes used for detection of reactive oxygen species. J Biochem Biophys Methods 65 (2005) 45-80
74. Hayakawa J., Kawamura T., Ohashi S., Horii T., and Watanabe Y. Habitat selection of Japanese top shell (Turbo cornutus) on articulated coralline algae; combination of preferences in settlement and post-settlement stage. J Exp Mar Biol Ecol 363 (2008) 118-123
75. De Zoysa M., Jung S., and Lee J. First molluscan TNF-α homologue of the TNF superfamily in disk abalone: molecular characterization and expression analysis. Fish Shellfish Immunol 26 (2009) 625-631
76. Nikapitiya C., De Zoysa M., and Lee J. Molecular characterization and gene expression analysis of a pattern recognition protein from disk abalone, Haliotis discus discus. Fish Shellfish Immunol 25 (2008) 638-647
77. Li X., Wang B., Liu S., and Xu J. The infection to a few kinds of shellfish inshore by a kind of virus. J Dalian Fish Univ 15 (2000) 86-91 [in Chinese with English abstract]
78. Zhengli S., and Handlinger J. Abalone viral mortality - disease card (2004), NACA, Bangkok, Thailand. http://library.enaca.org/Health/DiseaseLibrary/Abalone-Disease.pdf
79. Chang P.H., Kuo S.T., Lai S.H., Yang H.S., Ting Y.Y., Hsu C.L., et al. Herpes-like virus infection causing mortality of cultured abalone Haliotis diversicolor supertaxa in Taiwan. Dis Aquat Org 65 (2005) 23-27
80. Soudant P., Paillard C., Choquet G., Lambert C., Reid H.I., Marhic A., et al. Impact of season and rearing site on the physiological and immunological parameters of the manila clam Venerupis (= Tapes, = Ruditapes) philippinarum. Aquaculture 229 (2004) 401-418
81. Delaporte M., Soudant P., Lambert C., Jegaden M., Moal J., Pouvreau S., et al. Characterisation of physiological and immunological differences between Pacific oysters (Crassostrea gigas) genetically selected for high or low survival to summer mortalities and fed different rations under controlled conditions. J Exp Mar Biol Ecol 353 (2007) 45-57
82. Lambert C., Soudant P., Dégremont L., Delaporte M., Moal J., Boudry P., et al. Hemocyte characteristics in families of oysters, Crassostrea gigas, selected for differential survival during summer and reared in three sites. Aquaculture 270 (2007) 276-288
83. da Silva M.P., Comesaña P., Fuentes J., and Villalba A. Variability of haemocyte and haemolymph parameters in European flat oyster Ostrea edulis families obtained from brood stocks of different geographical origins and relation with infection by the protozoan Bonamia ostreae. Fish Shellfish Immunol 24 (2008) 551-563
84. Flye-Sainte-Marie J., Soudant P., Lambert C., Le Goïc N., Goncalvez M., Travers M.A., et al. Variability of the hemocyte parameters of Ruditapes philippinarum in the field during an annual cycle. J Exp Mar Biol Ecol 377 (2009) 1-11
85. Feng S.Y. Cellular defense mechanisms of oysters and mussels. Am Fish Soc Spec Publ 18 (1988) 153-168
86. Tiscar P.G., and Mosca F. Defense mechanisms in farmed marine molluscs. Vet Res Comm 28S1 (2004) 57-62
87. Hooper C., Day R., Slocombe R., Handlinger J., and Benkendorff K. Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish Shellfish Immunol 22 (2007) 363-379
88. Tripp M.R. Phagocytosis by hemocytes of the hard clam, Mercenaria mercenaria. J Invertebr Pathol 59 (1992) 222-227
89. López C., Carballal M.J., Azevedo C., and Villalba A. Differential phagocytic ability of the circulating haemocyte types of the carpet shell clam Ruditapes decussatus (Mollusca: Bivalvia). Dis Aquat Org 30 (1997) 209-215
90. Bettencourt R., Dando P., Collins P., Costa V., Allam B., and Serrão Santos R. Innate immunity in the deep sea hydrothermal vent mussel Bathymodiolus azoricus. Comp Biochem Physiol 152A (2009) 278-289
91. Luzio J.P., Pryor P.R., and Bright N.A. Lysosomes: fusion and function. Nat Rev Mol Cell Biol 8 (2007) 622-632
92. Wang T., Li X., Bott K., Song L., Clarke S., and Zhao W. Effects of water temperature on the lysosomal membrane stability in hemocytes of blacklip abalone, Haliotis rubra (Leach). J Shellfish Res 25 (2006) 935-940
93. Babior B.M., Kipnes R.S., and Curnutte J.T. Biological defence mechanisms: the production by leukocytes of superoxide, a potential bactericidal agent. J Clin Invest 52 (1973) 741-744
94. Klebanoff S.J. Antimicrobial mechanisms in neutrophilic polymorphonuclear leukocytes. Semin Hematol 12 (1975) 117-142
95. Gorbushin A.M., and Iakovleva N.V. Functional characterization of Littorina littorea (Gastropoda: Prosobranchia) blood cells. J Mar Biol Assoc UK 87 (2007) 741-746
96. Newton A.C. Protein kinase C: structure, function, and regulation. J Biol Chem 270 (1995) 28495-28498
97. Torreilles J., Guérin M.C., and Roch P. Reactive oxygen species and defense mechanisms in marine bivalves. C R Acad Sci Ser 319 (1996) 209-218 [in French]
98. Nakayama K., and Maruyama T. Differential production of active oxygen species in photo-symbiotic and non-symbiotic bivalves. Dev Comp Immunol 22 (1998) 151-159
99. Li H., Hu J., Xin W., and Zhao B. Production and interaction of oxygen and nitric oxide free radicals in PMA stimulated macrophages during the respiratory burst. Redox Rep 5 (2000) 353-358
100. Lambert C., Soudant P., Choquet G., and Paillard C. Measurement of Crassostrea gigas haemocyte oxidative metabolism by flow cytometry and the inhibiting capacity of pathogenic vibrios. Fish Shellfish Immunol 15 (2003) 225-240
101. Buggé M.D., Hégaret H., Wikfors G.H., and Allam B. Oxidative burst in hard clam (Mercenaria mercenaria) haemocytes. Fish Shellfish Immunol 23 (2007) 188-196
102. Conte A., and Ottaviani E. Nitric oxide synthase activity in molluscan hemocytes. FEBS Lett 365 (1995) 120-124
103. Aldieri E., Riganti C., Polimeni M., Gazzano E., Lussiana C., Campia I., et al. Classical inhibitors of NOX NAD(P)H oxidases are not specific. Curr Drug Metabol 9 (2008) 686-696
104. Stefanska J., and Pawliczak R. Apocynin: molecular aptitudes. Mediat Inflamm 2008 (2008) 106507
105. Lambert C., Soudant P., Jegaden M., Delaporte M., Labreuche Y., Moal J., et al. In vitro modulation of reactive oxygen and nitrogen intermediate (ROI/RNI) production in Crassostrea gigas hemocytes. Aquaculture 270 (2007) 413-421
106. 2+ pools. PNAS 100 (2003) 6157-6162
107. Aronis A., Melendez J.A., Golan O., Shilo S., Dicter N., and Tirosh O. Potentiation of Fas-mediated apoptosis by attenuated production of mitochondria-derived reactive oxygen species. Cell Death Diff 10 (2003) 335-344