Comparison of haemocytic parameters among flat oyster Ostrea edulis stocks with different susceptibility to bonamiosis and the Pacific oyster Crassostrea gigas

Journal of Invertebrate Pathology

Volumn 109, Issue 3, 2012, Pages 274-286

  Comesaña, Pilar ^a   Casas, Sandra M ^a,c   Cao, Asunción ^a,d   Abollo, Elvira ^a   Arzul, Isabelle ^b   Morga, Benjamin ^b   Villalba, Antonio ^a  

^a CENTRO DE INVESTIGACIÓNS MARIÑAS   (Spain)

^b IFREMER   (France)

^c LOUISIANA STATE UNIVERSITY   (United States)

^d Centro Tecnologico del Mar Fundacion CETMAR   (Spain)

Author keywords

Bonamia ostreae; Crassostrea gigas; Haemocyte; Nitric oxide; Ostrea edulis; Phagocytosis; Respiratory burst

Indexed keywords

HYDROGEN PEROXIDE; NITRIC OXIDE; SUPEROXIDE;

ANIMAL; ANIMAL PARASITOSIS; ARTICLE; BIOSYNTHESIS; BLOOD CELL; COMPARATIVE STUDY; DISEASE PREDISPOSITION; FLOW CYTOMETRY; HAPLOSPORIDIA; IMMUNOLOGY; METABOLISM; OYSTER; PARASITOLOGY; PHAGOCYTOSIS;

ANIMALS; DISEASE SUSCEPTIBILITY; FLOW CYTOMETRY; HAPLOSPORIDA; HEMOCYTES; HYDROGEN PEROXIDE; NITRIC OXIDE; OSTREIDAE; PHAGOCYTOSIS; PROTOZOAN INFECTIONS, ANIMAL; SUPEROXIDES;

BONAMIA (HAPLOSPORIDA); BONAMIA OSTREAE; CRASSOSTREA GIGAS; HAPLOSPORIDIA; OSTREA EDULIS; OSTREIDAE; PROTOZOA;

EID: 84857444237     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2011.12.007     Document Type: Article

References (106)

1. Adema C.M., van der Knaap W.P.W., Sminia T. Molluscan hemocyte-mediated cytotoxicity: the role of reactive oxygen intermediates. Rev. Aquat. Sci. 1991, 4:201-223.
2. Adema C.M., van Deutekom-Mulder E.C., van der Knaap W.P.W., Meuleman E.A., Sminia T. Generation of oxygen radicals in hemocytes of the snail Lymnaea stagnalis in relation to the rate of phagocytosis. Dev. Comp. Immunol. 1991, 15:17-26.
3. Aladaileh S., Nair S.V., Birch D., Raftos D.A. Sydney rock oyster (Saccostrea glomerata) hemocytes: morphology and function. J. Invertebr. Pathol. 2007, 96:48-63.
4. Allam B., Ford S.E. Effects of the pathogenic Vibrio tapetis on defence factors of susceptible and non-susceptible bivalves species: I. Haemocytes changes following in vitro challenge. Fish Shellfish Immunol. 2006, 20:374-383.
5. Allam B., Ashton-Alcox K.A., Ford S.E. Haemocyte parameters associated with resistance to brown ring disease in Ruditapes spp. clams. Dev. Comp. Immunol. 2001, 25:365-375.
6. Anderson R.S. Hemocyte-derived reactive oxygen intermediate production in four bivalve mollusks. Dev. Comp. Immunol. 1994, 18:89-96.
7. Anderson R.S., Burreson E.M., Paynter K.T. Defense responses of hemocytes withdrawn from Crassostrea virginica infected with Perkinsus marinus. J. Invertebr. Pathol. 1995, 66:82-89.
8. Arumugam M., Romestand B., Torreilles J. Nitrite released in haemocytes from Mytilus galloprovincialis, Crassostrea gigas and Ruditapes decussatus upon stimulation with phorbol myrstate acetate. Aquat. Living Resour. 2000, 13:173-177.
9. Arzul I., Langlade A., Chollet B., Robert M., Ferrand S., Omnes E., Lerond S., Couraleau Y., Joly J.P., François C., Garcia C. Can the protozoan parasite Bonamia ostreae infect larvae of flat oysters Ostrea edulis?. Vet. Parasitol. 2011, 179:69-76.
10. Auffret M. Comparative study of the hemocytes of two oyster species: the European flat oyster, Ostrea edulis, Linnaeus, 1750 and the pacific oyster, Crassostrea gigas (Thunberg, 1793). J. Shellfish Res. 1989, 8:367-373.
11. Babior B.M. Superoxide: a two-edged sword. Bra. J. Med. Biol. Res. 1997, 30:141-155.
12. Bachère E., Chagot D., Grizel H. Cell separation by centrifugal elutriation. Am. Fish. Soc. Spec. Publ. 1988, 18:281-285.
13. Bachère E., Hervio D., Mialhe E. Luminol-dependent chemiluminescence by hemocytes of two marine bivalves, Ostrea edulis and Crassostrea gigas. Dis. Aquat. Org. 1991, 11:173-180.
14. Bachère E., Mialhe E., Noel D., Boulo V., Morvan A., Rodríguez J. Knowledge and research prospects in marine mollusc and crustacean immunology. Aquaculture 1995, 132:17-32.
15. Badwey J.A., Karnovsky M.L. Active oxygen species and the functions of phagocytic leukocytes. Ann. Rev. Biochem. 1980, 49:695-726.
16. Balouet G., Poder M., Cahour A. Haemocytic parasitosis: morphology and pathology of lesions in the French flat oyster, Ostrea edulis L. Aquaculture 1983, 34:1-14.
17. Balseiro P., Fernández Conchas R., Montes J., Gómez-León J., Novoa B., Figueras A. Comparison of diagnosis techniques for the protozoan parasite Bonamia ostreae in flat oyster Ostrea edulis. Aquaculture 2006, 261:1135-1143.
18. Cao A., Fuentes J., Comesaña P., Casas S.M., Villalba A. A proteomic approach envisaged to analyse the bases of oyster tolerance/resistance to bonamiosis. Aquaculture 2009, 295:149-156.
19. Chagot, D.J., 1989. Caracterisation morphologique et functionelle des hemocytes d'Ostrea edulis et de Crassostrea gigas, mollusques bivalves. Etude in vitro de leurs interactions avec le protozoaire Bonamia ostreae (Ascetospora). Thèse du diplome de l'Ecole Pratique des Hautes Etudes, Université de Montpellier, France.
20. Chagot D., Boulo V., Hervio D., Mialhe E., Bachère E., Mourton C., Grizel H. Interactions between Bonamia ostreae Protozoa: (Ascetospora) and hemocytes of Ostrea edulis and Crassostrea gigas (Mollusca: Bivalvia): entry mechanisms. J. Invertebr. Pathol. 1992, 59:241-249.
21. Chakravortty D., Hensel M. Inducible nitric oxide synthase and control of intracellular bacterial pathogens. Microbes Infect. 2003, 5:621-627.
22. Chang S.-J., Tseng S.-M., Chou H.-Y. Morphological characterization via light and electron microscopy of the hemocytes of two cultured bivalves: a comparison study between the hard clam (Meretrix lusoria) and Pacific oyster (Crassostrea gigas). Zool. Sci. 2005, 44:144-152.
23. Cheng T.C. Bivalves. Invertebrate Blood Cells 1981, 233-300. Academic Press, London, UK. N.A. Ratcliffe, A.F. Rowley (Eds.).
24. Cheng T.C. Hemocytes: forms and functions. The Eastern Oyster 1996, 299-333. Maryland Sea Grant, College Park, MD, USA. V.S. Kennedy, R.I.E. Newell, A.F. Eble (Eds.).
25. Cheng T.C. Cellular defense mechanisms in oysters. Recent Advances in Marine Biotechnology 2000, 43-83. Science Publishers, Enfield, NH, USA. M. Fingerman, R. Nagabhushanam (Eds.).
26. Chu F.-L.E. Defense mechanisms of marine bivalves. Recent Advances in Marine Biotechnology 2000, 1-42. Science Publishers, Enfield, NH, USA. M. Fingerman, R. Nagabhushanam (Eds.).
27. Chu F.-L.E., La Peyre J.F. Perkinsus marinus susceptibility and defense-related activities in eastern oysters Crassostrea virginica: temperature effects. Dis. Aquat. Org. 1993, 16:223-234.
28. Cima F., Matozzo V., Marin M.G., Ballarin L. Haemocytes of the clam Tapes philippinarum (Adams & Reeve, 1850): morphofunctional characterisation. Fish. Shellfish Immunol. 2000, 10:677-693.
29. Cochennec, N., 2001. Bonamia ostreae, parasite de l'huître plate,Ostrea edulis, sa position taxonomique parmi les parasites du groupe " Microcell," analyses des interactions hôte/parasite chez plusieurs populations d'huîtres plates. Thèse de Doctorat, Université de la Rochelle, France.
30. Cochennec N., Garcia S. Flow cytometric comparison of esterase and radicals oxygen intermediate productions by Ostrea edulis haemocytes uninfected and infected by the protistan parasite Bonamia ostreae. J. Eukaryot. Microbiol. 2000, 48:16A-17A.
31. Cochennec, N., Renault, T., Chollet, B., Maffart, P., 1995. Comparison of haemograms from resistant and susceptible European flat oysters, Ostrea edulis, exposed to the parasite Bonamia ostreae. In: Abstracts Book of the 7th International Conference " Disease of Fish and Shellfish" Eur. Assoc. Fish Pathologists, Palma de Mallorca, Spain, p. 17 (10-15 September).
32. Cochennec N., le Roux F., Berthe F., Gerard A. Detection of Bonamia ostreae based on small subunit ribosomal probe. J. Invertebr. Pathol. 2000, 76:26-32.
33. Cochennec-Laureau N., Auffret M., Renault T., Langlade A. Changes in circulating and tissue-infiltrating hemocyte parameters of European flat oysters, Ostrea edulis, naturally infected with Bonamia ostreae. J. Invertebr. Pathol. 2003, 83:23-30.
34. Conte A., Ottaviani E. Nitric oxide synthase activity in molluscan hemocytes. FEBS Lett. 1995, 365:120-124.
35. Culloty S.C., Novoa B., Pernas M., Longshaw M., Mulcahy M.F., Feist S.W., Figueras A. Susceptibility of a number of bivalve species to the protozoan parasite Bonamia ostreae and their ability to act as vectors for this parasite. Dis. Aquat. Org. 1999, 37:73-80.
36. Culloty S.C., Cronin M.A., Mulcahy M.F. An investigation into the relative resistance of Irish flat oysters Ostrea edulis L. to the parasite Bonamia ostreae (Pichot et al., 1980). Aquaculture 2001, 199:229-244.
37. Culloty S.C., Cronin M.A., Mulcahy M.F. Potential resistance of a number of populations of the oyster Ostrea edulis to the parasite Bonamia ostreae. Aquaculture 2004, 237:41-58.
38. da Silva P.M., Villalba A. Comparison of light microscopic techniques for the diagnosis of the infection of the European flat oyster Ostrea edulis by the protozoan Bonamia ostreae. J. Invertebr. Pathol. 2004, 85:97-104.
39. da Silva P.M., Fuentes J., Villalba A. Growth, mortality and disease susceptibility of oyster Ostrea edulis families obtained from brood stocks of different geographical origins, through on growing in the Ría de Arousa (Galicia, NW Spain). Mar. Biol. 2005, 147:965-977.
40. da Silva P.M., Comesaña P., Fuentes J., 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. 2008, 24:551-563.
41. Dermine J.-F., Desjardins M. Survival of intracellular pathogens within macrophages. Protoplasma 1999, 210:11-24.
42. Elston R.A., Kent M.L., Wilkinson M.T. Resistance of Ostrea edulis to Bonamia ostreae infection. Aquaculture 1987, 64:237-242.
43. Faisal M., MacIntyre E.A., Adham K.G., Tall B.D., Kothary M.H., La Peyre J.F. Evidence for the presence of protease inhibitors in eastern (Crassostrea virginica) and Pacific (Crassostrea gigas) oyster. Comp. Biochem. Physiol. B 1998, 121:161-168.
44. Feng S.Y. Cellular defense mechanisms of oysters and mussels. Am. Fish. Soc. Spec. Publ. 1988, 18:153-168.
45. Fisher W.S. In vitro binding of parasites Bonamia ostreae and latex particles by hemocytes of susceptible and insusceptible oysters. Dev. Comp. Immunol. 1988, 12:43-53.
46. Ford S.E., Kanaley S.A., Littlewood D.T.J. Cellular responses of oysters infected with Haplosporidium nelsoni: changes in circulating and tissue-infiltrating hemocytes. J. Invertebr. Pathol. 1993, 61:49-57.
47. Franchini A., Fontanili P., Ottaviani E. Invertebrate immunocytes: relationship between phagocytosis and nitric oxide production. Comp. Biochem. Physiol. B 1995, 110:403-407.
48. Fryer S.E., Bayne C.J. Host-parasite interactions in molluscs. Invertebrate Immunology 1996, 131-153. Springer Verlag, Heidelberg, Germany. B. Rinkevich, W.E.G. Müller (Eds.).
49. Gauthier J.D., Vasta G.R. Effects of plasma from bivalve mollusk species on the in vitro proliferation of the protistan parasite Perkinsus marinus. J. Exp. Zool. 2002, 292:221-230.
50. Goedken M., Morsey B., Sunila I., de Guise S. Immunomodulation of Crassostrea gigas and Crassostrea virginica cellular defense mechanisms by Perkinsus marinus. J. Shellfish Res. 2005, 24:487-496.
51. Gourdon I., Guerin M.-C., Torreilles J., Roch P. Nitric oxide generation by hemocytes of the mussel Mytilus galloporvincialis. Biol. Chem. 2001, 5:1-6.
52. Gruenberg J., van der Goot F.G. Toxoplasma: guess who's coming to dinner. Cell 2006, 125:226-228.
53. Guerin M.-C., Torreilles J. Production of peroxynitrite by zymosan stimulation of Mytilus galloprovincialis haemocytes in vitro. Fish Shellfish Immunol. 1999, 9:509-518.
54. Hahn U.K., Bender R.C., Bayne C.J. Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata. J. Parasitol. 2001, 87:778-785.
55. Hervio, D., 1992. Contribution a l'etude de Bonamia ostreae (Ascetospora), protozoaire parasite de l'huitre Ostrea edulis (Bivalvia), et a l'analyse des interactions hote-parasite. Ph D Thesis, Blaise Pascal University, Clermont Ferrand, France.
56. Hervio D., Bachère E., Mialhe E., Grizel H. Chemiluminescent responses of Ostrea edulis and Crassostrea gigas hemocytes to Bonamia ostreae (Ascetospora). Dev. Comp. Immunol. 1989, 13:449.
57. Hervio D., Chagot D., Grizel H., Mialhe E., Goldin P. Localization and characterization of acid phosphatase activity in Bonamia ostreae (Ascetospora), an intrahemocytic protozoan parasite of the flat oyster Ostrea edulis (Bivalvia). Dis. Aquat. Org. 1991, 12:67-70.
58. Hervio D., Bachère E., Boulo V., Cochennec N., Vuillemin V., Le Coguic Y., Cailletaux G., Mazurie J., Mialhe E. Establishment of an experimental infection protocol for the flat oyster, Ostrea edulis, with the intrahaemocytic protozoan parasite, Bonamia ostrae: application in the selection of parasite-resistant oysters. Aquaculture 1995, 132:183-194.
59. Hine P.M. The inter-relations of bivalve haemocytes. Fish Shellfish Immunol. 1999, 9:367-385.
60. Howard D.W., Smith C.S. Histological techniques for bivalve mollusks. NOAA technical memorandum NMFS-F/NEC-25 1983, Woods Hole, MA, USA.
61. Huffman J.E., Tripp M.R. Cell-types and hydrolytic enzymes of soft shell clam (Mya arenaria) Hemocytes. J. Invertebr. Pathol. 1982, 40:68-74.
62. Ischiropoulos H., Zhu L., Beckman J.S. Peroxynitrite formation from macrophage-derived nitric oxide. Arch. Biochem. Biophys. 1992, 298:446-451.
63. James S.L. Role of nitric oxide in parasitic infections. Microbiol. Rev. 1995, 59:533-547.
64. Kimura H., Sawada T., Oshima S., Kozawa K., Ishioka T., Kato M. Toxicity and roles of reactive oxygen species. Current drug targets. Inflamm. Allergy 2005, 4:489-495.
65. Kwok, L.Y., Schlüter, D., Clayton, C., Soldati, D., 2004. Erratum (in Mol. Microbiol. 2005. 58, 915. Ding, Martina added. The antioxidant systems in Toxoplasma gondii and the role of cytosolic catalase in defence against oxidative injury. Mol. Microbiol. 51, 47-61).
66. La Peyre J.F., Chu F.-L.E., Vogelbein W.K. In vitro interaction of Perkinsus marinus merozoites with eastern and Pacific oyster hemocytes. Dev. Comp. Immunol. 1995, 19:291-304.
67. Lacoste A., Malham S.K., Gelebart F., Cueff A., Poulet S.A. Stress-induced immune changes in the oyster Crassostrea gigas. Dev. Comp. Immunol. 2002, 26:1-9.
68. 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.
69. Lynch S.A., Armitage D.V., Wylde S., Mulcahy M.F., Culloty S.C. The susceptibility of young prespawning oysters, Ostrea edulis, to Bonamia ostreae. J. Shellfish Res. 2005, 24:1019-1025.
70. Lynch S.A., Abollo E., Ramilo A., Cao A., Culloty S.C., Villalba A. Observations raise the question if the Pacific oyster, Crassostrea gigas, can act as either a carrier or a reservoir for Bonamia ostreae or Bonamia exitiosa. Parasitology 2010, 137:1515-1526.
71. Martín-Gómez L., Villalba A., Abollo E. Molecular identification and expression study of genes involved in the immune response of the flat oyster Ostrea edulis against the bonamiosis. Gene 2012, 492:81-93.
72. Mialhe E., Bachère E., Chagot D., Grizel H. Isolation and purification of the protozoan Bonamia ostreae (Pichot et al. 1980), a parasite affecting the flat oyster Ostrea edulis. Aquaculture 1988, 71:293-299.
73. Mitta G., Vandenbulcke F., Roch P. Original involvement of antimicrobial peptides in mussel innate immunity. FEBS Lett. 2000, 486:185-190.
74. Montes J. Lag time for infestation of flat oyster (Ostrea edulis L.) by Bonamia ostrae in estuaries of Galicia. Aquaculture 1991, 93:235-239.
75. Montes J., Acosta C.P., Guerra A. Oyster mortality in Galicia (NW Spain). Aquaculture a Biotechnology in Progress 1989, 941-948. European Aquaculture Society, Bredene, Belgium. N. De Pauw, E. Jaspers, H. Ackefors, N. Wilkins (Eds.).
76. Morga B., Arzul I., Chollet B., Renault T. Infection with the protozoan parasite Bonamia ostreae modifies in vitro haemocyte activities of flat oyster Ostrea edulis. Fish Shellfish Immunol. 2009, 26:836-842.
77. Morga B., Renault T., Faury N., Chollet B., Arzul I. Cellular and molecular responses of haemocytes from Ostrea edulis during in vitro infection by the parasite Bonamia ostreae. Int. J. Parasitol. 2011, 41:755-764.
78. Morga B., Renault T., Faury N., Chollet B., Arzul I. Cellular and molecular responses of haemocytes from Ostrea edulis during in vitro infection by the parasite Bonamia ostreae. Int J. Parasitol. 2011, 41:755-764.
79. Mourton C., Boulo V., Chagot D., Hervio D., Bachère E., Mialhe E., Grizel H. Interactions between Bonamia ostreae (Protozoa: Ascetospora) and Hemocytes of Ostrea edulis and Crassostrea gigas (Mollusca: Bivalvia): in Vitro Sistem Establishment. J. Invertebr. Pathol. 1992, 59:235-240.
80. Müller S. Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol. Microbiol. 2004, 53:1291-1305.
81. Naciri-Graven Y., Martin A.G., Baud J.-P., Renault T., Gerard A. Selecting the flat oyster Ostrea edulis (L.) for survival when infected with the parasite Bonamia ostreae. J. Exp. Mar. Biol. Ecol. 1998, 224:91-107.
82. Naciri-Graven Y., Haure J., Gerard A., Baud J.-P. Comparative growth of Bonamia ostreae resistant and wild flat oyster Ostrea edulis in an intensive system II. Second year of the experiment. Aquaculture 1999, 171:195-208.
83. Nakayama K., Maruyama T. Differential production of active oxygen species in photo-symbiotic and non symbiotic bivalves. Dev. Comp. Immunol. 1998, 22:151-159.
84. Novas A., Cao A., Barcia R., Ramos-Martinez J.I. Nitric oxide release by hemocytes of the mussel Mytilus galloprovincialis Lmk was provoked by interleukin-2 but not by lipopolysaccharide. Int. J. Biochem. Cell. B 2004, 36:390-394.
85. Ottaviani E., Paemen L.R., Cadet P., Stefano G.B. Evidence for nitric oxide production and utilization as a bacteriocidal agent by invertebrate immunocytes. Eur. J. Pharm. Environ. 1993, 248:319-324.
86. Oubella R., Maes P., Paillard C., Auffret M. Experimentally-induced variation in hemocyte density for Ruditapes philippinarum and R. decussatus (Mollusca, Bivalvia). Dis. Aquat. Organ. 1993, 15:193-197.
87. Oubella R., Maes P., Allam B., Paillard C., Auffret M. Selective induction of hemocytic response in Ruditapes philippinarum (Bivalvia) by different species of Vibrio (Bacteria). Aquat. Living Resour. 1996, 9:137-143.
88. Pacher P., Beckman J.S., Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87:315-424.
89. Parry H.E., Pipe R.K. Interactive effects of temperature and copper on immunocompetence and disease susceptibility in mussels (Mytilus edulis). Aquat. Toxicol. 2004, 69:311-325.
90. Pichot Y., Comps M., Tigé G., Grizel H., Rabouin M.-A. Recherches sur Bonamia ostreae gen. n., sp. n., parasite nouveau de ĺhuitre plate Ostrea edulis L. Rev. Trav. Inst. Pe{ogonek}ches Marit. 1980, 43:131-140.
91. Pick E., Keisari Y. A simple colorimetric method for the measurement of hydrogen peroxide produced by cells in culture. J. Immunol. Meth. 1980, 38:161-170.
92. Pipe R.K. Generation of reactive oxygen metabolites by the haemocytes of the mussel Mytilus edulis. Dev. Comp. Immunol. 1992, 16:111-122.
93. Pipe R.K., Porte C., Livingstone D.R. Antioxidant enzymes associated with the blood cells and haemolymph of the mussel Mytilus edulis. Fish Shellfish Immunol. 1993, 3:221-233.
94. Polanco E., Montes J., Outon M.J., Melendez M.I. Situation pathologique du stock d́huitres plaes en Galice (Espagne) en relation avec Bonamia ostreae. Haliotis 1984, 14:91-95.
95. Reeves E.P., Nagl M., Godovac-Zimmermann J., Segal A.W. Reassessment of the microbicidal activity of reactive oxygen species and hypochlorous acid with reference to the phagocytic vacuole of the neutrophil granulocyte. J. Med. Microbiol. 2003, 52:643-651.
96. Reid H.I., Soudant P., Lambert C., Paillard C., Birkbeck T.H. Salinity effects on immune parameters of Ruditapes philippinarum challenged with Vibrio tapetis. Dis. Aquat. Org. 2003, 56:249-258.
97. Renault T., Cochennec N., Grizel H. Bonamia ostreae, parasite of the European flat oyster, Ostrea edulis, does not experimentally infect the Japanese oyster, Crassostrea gigas. Bull. Eur. Ass. Fish Pathol. 1995, 15:78-80.
98. Renault T., Xue Q., Chilmonczyk S. Flow cytometric analysis of European flat oyster, Ostrea edulis, haemocytes using a monoclonal antibody specific for granulocytes. Fish Shellfish Immunol. 2001, 11:269-274.
99. Romestand B., Torreilles J. Etude de la resiteance de l'huitre Crassostrea gigas face a la protozoose a Perkinsus marinus. Haliotis 2002, 31:21-32.
100. Roos D., van Bruggen R., Meischl C. Oxidative killing of microbes by neutrophils. Microbes Infect. 2003, 5:1307-1315.
101. Schott E.J., Robledo J.-A., Wright A.C., Silva A.M., Vasta G.R. Gene organization and homology modeling of two iron superoxide dismutases of the early branching protist Perkinsus marinus. Gene 2003, 309:1-9.
102. Schott E.J., Pecher W.T., Okafor F., Vasta G.R. The protistan parasite Perkinsus marinus is resistant to selected reactive oxygen species. Exp. Parasitol. 2003, 105:232-240.
103. Tafalla C., Novoa B., Figueras A. Production of nitric oxide by mussel (Mytilus galloprovincialis) hemocytes and effect of exogenous nitric oxide on phagocytic functions. Comp. Biochem. Physiol. B 2002, 132:423-431.
104. Tafalla C., Gomez-León J., Novoa B., Figueras A. Nitric oxide production by carpet shell clam (Ruditapes decussatus) hemocytes. Dev. Comp. Immunol. 2003, 27:197-205.
105. Volety A.K., Chu F.L.E. Suppression of chemiluminescence of eastern oyster (Crassostrea virginica) hemocytes by the protozoan parasite Perkinsus marinus. Dev. Comp. Immunol. 1995, 19:135-142.
106. Xue Q., Renault T., Cochennec N., Gerard A. Separation of European flat oyster, Ostrea edulis, haemocytes by density gradient centrifugation and SDS-PAGE characterisation of separated haemocyte sub-populations. Fish Shellfish Immunol. 2000, 10:155-165.