Protease activity in the plasma of American oysters, Crassostrea virginica, experimentally infected with the protozoan parasite Perkinsus marinus

Journal of Parasitology

Volumn 89, Issue 5, 2003, Pages 941-951

  Munoz P ^a,b   Vance, K ^a   Gomez Chiarri M ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

^b UNIVERSITY OF MURCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GELATIN; METALLOPROTEINASE; SERINE PROTEINASE;

ENZYME ACTIVITY; HOST-PARASITE INTERACTION; MOLLUSC; PARASITOLOGY; PROTOZOAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; BLOOD CELL; BLOOD SAMPLING; CONCENTRATION (PARAMETERS); CONFERENCE PAPER; CONTROLLED STUDY; ENZYME ACTIVITY; GEL ELECTROPHORESIS; INJECTION; MOLECULAR INTERACTION; MOLECULAR WEIGHT; NONHUMAN; OYSTER; PARASITE; PARASITOSIS; PERKINSUS MARINUS; PREVALENCE; PROTOZOAL INFECTION; PROTOZOON; STATISTICAL SIGNIFICANCE;

ANIMALS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPEPTIDASES; GELATIN; HEMOLYMPH; HOST-PARASITE RELATIONS; OSTREIDAE; PROTOZOA;

ANIMALIA; BIVALVIA; CRASSOSTREA; CRASSOSTREA VIRGINICA; MOLLUSCA; OSTREIDAE; PERKINSUS; PERKINSUS MARINUS; PROTOZOA;

EID: 0345714969     PISSN: 00223395     EISSN: None     Source Type: Journal    
DOI: 10.1645/GE-3126     Document Type: Conference Paper

References (68)

1. 2-macroglobulin activity in the plasma of mollusks. Veliger 35: 161-164.
2. BRADFORD, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
3. BRAUN-BRETON, C., AND D. S. PEREIRA. 1988. Activation of a Plasmodium falciparum protease correlated with merozoite maturation and erythrocyte invasion. Biology of the Cell 64: 223-231.
4. BRICELJ, V. M., S. E. FORD, F. J. BORRERO, F. O. PERKINS, G. RIVARA, R. E. HILLMAN, R. A. ELSTON, AND J. CHANG. 1992. Unexplained mortalities of hatchery-reared, juvenile oysters, Crassostrea virginica (Gmelin). Journal of Shellfish Research 11: 331-347.
5. BUSHEK, D., S. K. ALLEN, K. A. ALCOX, R. G. GUSTAFSON, AND S. E. FORD. 1997. Response of Crassostrea virginica to in vitro culture Perkinsus marinus: Preliminary comparisons of three inoculation methods. Journal of Shellfish Research 16: 479-485.
6. CHENG, T. C. 1988. Strategies employed by parasites of marine bivalves to effect successful establishment in hosts. American Fisheries Society Special Publications 18: 112-129.
7. -. 1996. Hemocytes: Forms and functions. In The Eastern oyster Crassostrea virginica, V. S. Kennedy, R. I. Newell, and A. E. Eble (eds.). Maryland Sea Grant Program, College Park, Maryland, p. 299-333.
8. CHINTALA, M. M., D. BUSHEK, AND S. E. FORD. 2002. Comparison of in vitro-cultured and wild-type Perkinsus marinus. II. Dosing methods and host response. Diseases of Aquatic Organisms 51: 203-216.
9. CORRADIN, S., A. RANSIJN, G. CORRADIN, J. BOUVIER, M. B. DELGADO, J. FERNANDEZ-CARNEADO, J. C. MOTTRAM, G. VERGERES, AND J. MAUEL. 2002. Novel peptide inhibitors of Leishmania gp63 based on the cleavage site of MARCKS-related protein. Biochemistry Journal 367: 761-769.
10. -, -, -, M. A. ROGGERO, A. A. SCHMITZ. P. SCHNEIDER, J. MAUEL, AND G. VERGERES. 1999. MARCKS-related protein (MRP) is a substrate for the Leishmania major surface protease leishmanolysin (gp63). Journal of Biological Chemistry 274: 25411-25418.
11. DARMON, A. J., AND R. C. BLEACKLEY. 1998. Proteases and cell-mediated cytotoxicity. Critical Reviews in Immunology 18: 255-273.
12. DRUILHE, P., P. HAGAN, AND G. A. W. ROOK. 2002. The importance of models of infection in the study of disease resistance. Trends in Microbiology 10: s38-s46.
13. DUNGAN, C. E., R. M. HAMILTON, E. M. BURRESON, AND L. M. RAGONE CALVO. 1996. Identification of Perkinsus marinus portals of entry by histochemical immunoassays of challenged oysters. Journal of Shellfish Research 15: 500.
14. ELSAYED, E. E., S. M. MCLAUGHLIN, AND M. FAISAL. 1999. Protease inhibitors in plasma of the softshell clam Mya arenaria: Identification and effects of disseminated sarcoma. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 123: 427-435.
15. FAISAL, M., E. A. MACINTYRE, K. G. ADHAM, B. D. TALL, M. H. KOTHARY, AND J. F. LA PEYRE. 1998. Evidence for the presence of protease inhibitors in Eastern (Crassostrea virginica) and Pacific (Crassostrea gigas) oysters. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 121: 161-168.
16. -, J. L. OLIVER, AND S. L. KAATTARI. 1999. Role of protease-antiprotease interactions in Perkinsus marinus infection in Crassostrea spp. Bulletin of the European Association of Fish Pathologists 19: 269-276.
17. -, D. Y. SCHAFHAUSER, K. A. GARREIS, E. ELSAYED, AND J. F. LA PEYRE. 1999. Isolation and characterization of Perkinsus marinus proteases using bacitracin-sepharose affinity chromatography. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 123: 417-426.
18. FINESCHI, B., AND J. MILLER. 1997. Endosomal proteases and antigen processing. Trends in Biochemical Sciences 22: 377-382.
19. FORD, S. E., M. M. CHINTALA. AND D. BUSHEK. 2002. Comparison of in vitro-cultured and wild-type Perkinsus marmus. I. Pathogen virulence. Diseases of Aquatic Organisms 51: 187-201.
20. -, AND M. R. TRIPP. 1996. Diseases and defense mechanisms. In The Eastern oyster, Crassostrea virginica, V. S. Kennedy, R. I. Newell, and A. E. Eble (eds.). Maryland Sea Grant, College Park, Maryland, p. 581-660.
21. GARREIS, K. A., J. F. LA PEYRE, AND M. FAISAL. 1996. The effects of Perkinsus marinus extracellular products and purified proteases on oyster defense parameters in vitro. Fish and Shellfish Immunology 6: 581-597.
22. GAUTHIER, J. D., AND G. R. VASTA. 1993. Continuous in vitro culture of the Eastern oyster parasite Perkinsus marinus. Journal of Invertebrate Pathology 62: 321-323.
23. HEUSSEN, C., AND E. B. DOWDLE. 1980. Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Analytical Biochemistry 102: 196-202.
24. IIDA, Y., T. NAKAGAWA, AND F. NAGOYAMA. 1991. Properties of collagenolytic proteinase in Japanese spiny lobster and horsehair crab Hepatopancreas. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 98: 403-410.
25. KLEMBA, M., AND D. E. GOLDBERG. 2002. Biological roles of proteases in parasitic protozoa. Annual Reviews in Biochemistry 71: 275-305.
26. LA PEYRE, J. F., D. Y. SCHAFHAUSER, E. H. RIZKALLA, AND M. FAISAL. 1995. Production of serine proteases by the oyster pathogen Perkinsus marinus (Apicomplexa) in vitro. Journal of Eukaryotic Microbiology 42: 544-551.
27. -, H. A. YARNALL, AND M. FAISAL. 1996. Contribution of Perkinsus marinus extracellular products in the infection of Eastern oysters (Crassostrea virginica). Journal of Invertebrate Pathology 68: 312-313.
28. LLANO, E., A. M. PENDAS, P. AZA-BLANC. T. B. KORNBERG, AND C. LOPEZ-OTIN. 2000. Dm1-MMP, a matrix metalloproteinase from Drosophila with a potential role in extracellular matrix remodeling during neural development. Journal of Biological Chemistry 275: 35978-35985.
29. MACINTYRE, E. A., C. G., EARNHART, AND S. L. KAATTARI. 2003. Host oyster tissue extracts modulate in vitro protease expression and cellular differentiation in the protozoan parasite, Perkinsus marinus. Parasitology 126: 293-302.
30. MACKIN, J. G. 1951. Histopathology of infection of Crassostrea virginica (Gmelin) by Dermocystidium marinum Mackin, Oven, and Collier. Bulletin of Marine Science of the Gulf and Caribbean 1: 72-87.
31. -. 1962. Oyster diseases caused by Dermocystidium marinum and other microorganisms in Louisiana. Publications of the Institute of Marine Sciences University of Texas 7: 132-229.
32. -, AND J. L. BOSWELL. 1955. The life cycle and relationships of Dermocystidium marinum. Proceedings of the National Shellfisheries Association 46: 112-115.
33. MANNELLO, F., L. CANESI, G. GAZZANELLL, AND G. GALLO. 2001. Biochemical properties of metalloproteinases from the hemolymph of the mussel Mytilus galloprovincialis Lam. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 128: 507-515.
34. MARDEN, P. A., A. K. TUNLID, K. G. MALMCRONA-FRIBERG, G. ODHAM, AND S. KJELLEBERG. 1985. Physiological and morphological changes during short term starvation of marine bacteriological isolates. Archives in Microbiology 142: 326-332.
35. MAREIRO, K. L. 2002. A survey of disease in two commercially important bivalves in Rhode Island (1998-2001). M.S. Thesis. University of Rhode Island, Kingston, Rhode Island, 144 p.
36. MARSH, A. G., J. D. GAUTHIER, AND G. R. VASTA. 1995. A semiquantitative PCR assay for assessing Perkinsus marinus infections in the Eastern oyster. Crassostrea virginica. Journal of Parasitology 81: 577-583.
37. MARTINEZ, J., AND J. J. CAZZULO. 1992. Anomalous electrophoretic behaviour of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi in relation to its apparent molecular mass. FEMS Microbiology Letters 74: 225-229.
38. MASSOVA, I., L. P. KOTRA, R. FRIDMAN, AND S. MOBASHERY. 1998. Matrix metalloproteinases: Structures, evolution, and diversification. FASEB Journal 12: 1075-1095.
39. MCKERROW, J. H., E. SUN, P. J. ROSENTHAL, AND J. BOUVIER. 1993. The proteases and pathogenicity of parasitic protozoa. Annual Reviews in Microbiology 47: 821-853.
40. MCLAUGHLIN, S. M., E. E. ELSAYED, AND M. FAISAL. 2000. Analysis of extracellular proteins of two Perkinsus spp. isolated from the soft-shell clam Mya arenaria in vitro. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 126: 587-598.
41. MEZA, I. 2000. Extracellular matrix-induced signaling in Entamoeba histolytica: Its role in invasiveness. Parasitology Today 16: 23-28.
42. MODHA, J., M. C. ROBERTS, AND J. R. KUSEL. 1996. Schistosomes and Serpins: A complex business. Parasitology Today 12: 119-121.
43. MONTAGNANI, C., F. LE ROUX, F. BERTHE, AND J. M. ESCOUBAS. 2001. Cg-TIMP, an inducible tissue inhibitor of metalloproteinase from the Pacific oyster Crassostrea gigas with a potential role in wound healing and defense mechanisms. FEBS Letters 500: 64-70.
44. NAGASE, H., AND J. F. WOESSNER. 1999. Matrix metalloproteinases. Journal of Biological Chemistry 274: 21491-21494.
45. NOREN, F., O. MOESTRUP, AND A.-S. REHNSTAM-HOLM. 1999. Parvilucifera infectans Noren et Moestrup gen. et sp. Nov. (Perkinsoa phylum nov.): A parasitic flagellate capable of killing toxic microalgae. European Journal of Protistology 35: 233-254.
46. OLIVER, J. L., P. M. GAFFNEY, S. K. ALLEN, M. FAISAL, AND S. L. KAATTARI. 2000. Protease inhibitory activity in selectively bred families of Eastern oysters. Journal of Aquatic Animal Health 12: 136-145.
47. -, T. D. LEWIS, M. FAISAL, AND S. L. KAATTARI. 1999. Analysis of the effects of Perkinsus marinus proteases on plasma proteins of the Eastern oyster (Crassostrea virginica) and the Pacific oyster (Crassostrea gigas). Journal of Invertebrate Pathology 74: 173-183.
48. ORDÁS, M. C., B. NOVOA, M. FAISAL, S. M. MCLAUGHLIN, AND A. FIGUERAS. 2001. Proteolytic activity of cultured Pseudoperkinsus tapetis extracellular products. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 130: 199-206.
49. OTTINGER, C., T. LEWIS, D. SHAPIRO, M. FAISAL, AND S. L. KAATTARI. 2001. Detection of Perkinsus marinus extracellular proteins in tissues of the Eastern oyster Crassostrea virginica: Potential use in diagnostic assays. Journal of Aquatic Animal Health 13: 133-141.
50. PERKINS, F. O. 1969. Ultrastructure of vegetative stages in Labyrinthomyxa marina (Dermocystidium marinum), a commercially significant oyster pathogen. Journal of Invertebrate Pathology 13: 199-222.
51. -. 1976. Dermocystidium marinum infection in oysters. Marine Fish Review 38: 19-21.
52. QUIGLEY, J. P., R. S. BRAITHWAITE, AND P. B. ARMSTRONG. 1993. Matrix metalloproteases of the developing sea urchin embryo. Differentiation 54: 19-23.
53. RAY, S. R. 1952. A culture technique for the diagnosis of infection with Dermocystidium marinum. Mackin, Oven, and Colliers in oysters. Science 116: 360-361.
54. -. 1966. A review of the cultured method for detecting Dermocystidium marinum, with suggested modifications and precautions. Proceedings of the National Shellfisheries Association 54: 55-69.
55. -, 1996. Historical perspective on Perkinsus marinus disease of oysters in the Gulf of Mexico. Journal of Shellfish Research 15: 9-11.
56. RHOADS, M. L., AND R. H. FETTERER. 1997. Extracellular matrix: A tool for defining the extracorporeal function of parasite proteases. Parasitology Today 13: 119-122.
57. ROBINSON, J. J. 1997. Characterization of a metalloproteinase: A late stage specific gelatinase activity in the sea urchin embryo. Journal of Cell Biochemistry 66: 337-345.
58. ROMESTAND, B., F. CORBIER, AND P. ROCH. 2002. Protease inhibitors and haemagglutinins associated with resistance to the protozoan parasite, Perkinsus marinus, in the Pacific oyster, Crassostrea gigas. Parasitology 125: 323-329.
59. ROSENTHAL, P. J., K. KIM, J. H. MCKERROW, AND J. H. LEECH. 1987. Identification of three stage-specific proteinases of Plasmodium falciparum. Journal of Experimental Medicine 166: 816-821.
60. SHAPIRO, S. D. 1998. Matrix metalloproteinase degradation of extracellular matrix: Biological consequences. Current Opinion in Cell Biology 10: 602-608.
61. SIM, R. B., AND A. LAICH. 2000. Serine proteases of the complement system. Biochemical Society Transactions 28: 545-550.
62. TALL, B. D., J. F. LA PEYRE, J. W. BIER, M. D. MILIOTIS, D. E. HANES, M. H. KOTHARY, D. B. SHAH, AND M. FAISAL. 1999. Perkinsus marinus extracellular protease modulates survival of Vibrio vulnificus in Eastern oyster (Crassostrea virginica) hemocytes. Applied and Environmental Microbiology 65: 4261-4263.
63. THOESSEN, J. C. 1994. Suggested procedures for the detection and identification of certain finfish and shellfish pathogens. 4th ed. Fish Health Section, American Fisheries Society, Fair Haven, New Jersey, 317 p.
64. VILLADANGOS, J. A., R. A. BRYANT. J. DEUSSING, C. DRIESSEN, A. M. LENNON-DUMENIL, R. J. RIESE, W. ROTH, P. SAFTIG, G. P. SHI, H. A. CHAPMAN, C. PETERS, AND H. L. PLOEGH. 1999. Proteases involved in MHC class II antigen presentation. Immunological Reviews 172: 109-120.
65. VOLETY, A., AND W. S. FISHER. 2000. In vitro killing of Perkinsus marinus by hemocytes of oysters Crassostrea virginica. Journal of Shellfish Research 19: 827-834.
66. WADA, K., H. SATO, H. KINOH, M. KAJITA, H. YAMAMOTO, AND M. SEIKI. 1998. Cloning of three Caenorhabditis elegans genes potentially encoding novel matrix metalloproteinases. Gene 211: 57-62.
67. WINDLE, H. J., AND D. KELLEHER. 1997. Identification and characterization of a metalloprotease activity from Helicobacter pylori. Infection and Immunity 65: 3132-3137.
68. ZIEGLER, G., K. PAYNTER, AND D. FISHER. 2002. Matrix metalloproteinase-like activity from hemocytes of the Eastern oyster, Crassostrea virginica. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 131: 361-370.