Serine protease inhibitor cvSI-1 potential role in the eastern oyster host defense against the protozoan parasite Perkinsus marinus

Developmental and Comparative Immunology

Volumn 34, Issue 1, 2010, Pages 84-92

  La Peyre, Jerome F ^a   Xue, Qing Gang ^a   Itoh, Naoki ^a   Li, Yanli ^a   Cooper, Richard K ^a  

^a LOUISIANA STATE UNIVERSITY AGRICULTURAL CENTER   (United States)

Author keywords

Bivalve mollusks; Crassostrea virginica; Dermo; Disease resistance; Genetic selection; In situ hybridization; Innate immunity; Plasma protein; Quantitative real time RT PCR

Indexed keywords

CRASSOSTREA VIRGINICA SERINE PROTEINASE INHIBITOR 1; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; BASOPHIL; BLOOD CELL; CONTROLLED STUDY; ENZYME ACTIVITY; EXOCRINE GLAND; GENE EXPRESSION; HOST RESISTANCE; IN SITU HYBRIDIZATION; IN VITRO STUDY; NONHUMAN; OYSTER; PERKINSUS MARINUS; PRIORITY JOURNAL; PROTOZOON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUMMER; WINTER;

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

EID: 70349985699     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2009.08.007     Document Type: Article

References (82)

1. Kanost M.R., and Jiang H. Proteinase inhibitors in invertebrate immunity. In: Söderhäll K., Iwanaga S., and Vasta G.R. (Eds). New directions in invertebrate immunology (1996), SOS Publications, Fair Haven, NJ 07704-3303 pp. 155-173
2. Kanost M.R. Serine protease inhibitors in arthropod immunity. Dev Comp Immunol 23 (1999) 291-301
3. Reichhart J.M. Tip of another iceberg: Drosophila serpins. Trends Cell Biol 15 (2005) 659-665
4. Iganawa S., and Lee B.L. Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38 (2006) 128-150
5. Cerenius L., Lee B.L., and Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29 (2008) 263-271
6. Miura Y., Kawabata S., and Iwanaga S. A Limulus intracellular coagulation inhibitor with characteristics of the serpin superfamilty. J Biol Chem 269 (1994) 542-547
7. Agarwara K.L., Kawabata S., Miura Y., Kuroki Y., and Iwanaga S. Limulus intracellular coagulation inhibitor type 3. Purification, characterization, cDNA cloning, and tissue localization. J Biol Chem 271 (1996) 23768-23774
8. Jiang H., and Kanost M.R. Characterization and functional analysis of twelve naturally occurring reactive site variants of serpin-1 from Manduca sexta. J Biol Chem 272 (1997) 1082-1087
9. Liang Z., Sottrup-Jensen L., Aspan A., Hall M., and Söderhäll K. Pacifastin, a novel 155-kDa heterodimeric proteinase inhibitor containing a unique transferring chain. Proc Natl Acad Sci USA 94 (1997) 6682-6687
10. Ligoxygakis P., Pekte N., Ji C., Leclerc V., Duvic B., Belvin M., et al. A serpin mutant links Toll activation to melanization in the host defence of Drosophila. EMBO J 21 (2002) 6330-6337
11. De Gregorio E., Han S.-J., Lee W.-J., Baek M.-J., Osaki T., Kawabata S., et al. An immune-responsive serpin regulates the melanization cascade in Drosophila. Dev Cell 3 (2002) 581-592
12. Tong Y., and Kanost M.R. Manduca sexta serpin-4 and serpin-5 inhibit the prophenoloxidase activation pathway. cDNA cloning, protein expression and characterization. J Biol Chem 280 (2005) 14923-14931
13. Levashina E.A., Langley E., Green C., Gubb D., Ashburner M., Hoffmann J.A., et al. Constitutive activation of Toll-mediated antifungal defense in serpin-deficient Drosophila. Science 285 (1999) 1917-1919
14. Salzet M., Vieau D., and Stefano G.B. Serpins: an evolutionary conserved survival strategy. Immunol Today 20 (1999) 541-544
15. Boucias D.G., and Pendland J.C. Detection of protease inhibitors in the hemolymph of resistant Anticarsia gemmatalis which are inhibitory to the entomopathogenic fungus, Nomuraca rileyi. Experientia 43 (1987) 336-339
16. Yoshida S., Yamashita M., Yonehara S., and Eguchi M. Properties of fungal protease inhibitors from the integument and haemolymph of the silkworm and effect of an inhibitor on the fungal growth. Comp Biochem Physiol Part B 95 (1990) 559-564
17. Vilcinskas A., and Wedde M. Inhibition of Beauveria bassiana proteases and fungal development by inducible protease inhibitors in the hemolymph of Galleria mellonella larvae. Biocont Sci Technol 7 (1997) 591-601
18. Fröbius A.C., Kanost M.R., Götz P., and Vilcinskas A. Isolation and characterization of novel inducible serine protease inhibitors from larval hemolymph of the greater wax moth Galleria mellonella. Eur J Biochem 267 (2000) 2046-2053
19. Abraham E.G., Pinto S.B., Ghosh A., Vanlandingham D.L., Budd A., Higgs S., et al. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc Natl Acad Sci USA 102 (2005) 16327-16332
20. Lantz M.S. Are bacterial proteases important virulence factors?. J Periodontal Res 32 (1997) 126-132
21. Klemba M., and Goldberg D.E. Biological roles of proteases in parasitic protozoa. Annu Rev Biochem 71 (2002) 275-305
22. McKerrow J.H., Caffrey C., Kelly B., Loke P., and Sajid M. Proteases in parasitic diseases. Annu Rev Pathol Mech Dis 1 (2006) 497-536
23. Bangalore N., Travis J., Onunka V.C., Pohl J., and Shafer W.M. Identification of the primary antimicrobial domains in human neutrophil cathepsin G. J Biol Chem 265 (1990) 13584-13588
24. Hiemstra P.S., Maassen R.J., Stolk J., Heinzel-Wieland R., Steffens G.J., and Dijkman J.H. Antibacterial activity of antileukoprotease. Infect Immun 64 (1996) 4520-4524
25. Sallenave J.M. Antimicrobial activity of antiproteinases. Biochem Soc Trans 30 (2002) 111-115
26. Yeamam M.R., and Yount N.Y. Unifying themes in host defense effector polypeptides. Nat Rev Microbiol 5 (2007) 727-740
27. Baranger K., Zani M.L., Chandenier J., Dallet-Choisy S., and Moreau T. The antibacterial and antifungal properties of trappin-2 (pre-elafin) do not depend on its protease inhibitory function. FEBS J 275 (2008) 2008-2020
28. Faisal M., MacIntyre E.A., Adham K.G., Tall B.D., Kothary M.H., and La Peyre J.F. Evidence for the presence of protease inhibitors in eastern (Crassostrea virginica) and Pacific (Crassotrea gigas) oysters. Comp Biochem Physiol Part B 121 (1998) 161-168
29. Romestand B., Corgier F., and Roch P. Protease inhibitors and haemagglutinins associated with resistance to the protozoan parasite, Perkinsus marinus, in the Pacific oyster, Crassostrea gigas. Parasitology 125 (2002) 323-329
30. Oliver J.L., Gaffney P.M., Allen Jr. S.K., Faisal M., and Kaattari S.L. Protease inhibitory activity in selectively bred families of eastern oysters. J Aquat Anim Health 12 (2000) 136-145
31. Montagnani C., Le Roux F., Berthe F., and Escoubas J.M. 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 Lett 500 (2001) 64-70
32. Zhu L., Song L., Chang Y., Xu W., and Wu L. Molecular cloning, characterization and expression of a novel serine proteinase inhibitor gene in bay scallop (Argopecten irradians, Lamarck 1819). Fish Shellfish Immunol 20 (2006) 320-331
33. Wang B., Zhao J., Song L., Zhang H., Wang L., Li C., et al. Molecular cloning and expression of a novel Kazal-type serine proteinase inhibitor gene from Zhikong scallop Chlamys farreri, and the inhibitory activity of its recombinant domain. Fish Shellfish Immunol 24 (2008) 629-637
34. Jenny M.J., Ringwood A.H., Lacy E.R., Lewitus A.J., Kempton J.W., Gross P.S., et al. Potential indicators of stress response identified by expressed sequence tag analysis of hemocytes and embryos from the American oyster, Crassostrea virginica. Mar Biotechnol 4 (2002) 81-93
35. Gueguen Y., Cadoret J.-P., Flament D., Barreau-Roumiguiere C., Girardot A.-L., Garnier J., et al. Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster, Crassostrea gigas. Gene 303 (2003) 139-145
36. Lang R.P., Bayne C.J., Camara M.D., Cunningham C., Jenny M.J., and Langdon C.J. Transcriptome profiling of selectively bred Pacific oyster Crassostrea gigas families that differ in tolerance of heat shock. Mar Biotechnol (2009) 10.1007/s10126-0009-9181-6
37. Roberts S., Goetz G., White S., and Goetz F. Analysis of genes isolated from plated hemocytes of the Pacific oyster, Crassostrea gigas. Mar Biotechnol 11 (2009) 24-44
38. Xue Q.G., Waldrop G.L., Schey K.L., Itoh N., Ogawa M., Cooper R.K., et al. A novel slow-tight binding serine protease inhibitor from eastern oyster (Crassostrea virginica) plasma inhibits perkinsin, the major extracellular protease of the oyster protozoan parasite Perkinsus marinus. Comp Biochem Physiol Part B 145 (2006) 16-26
39. La Peyre J.F., Faisal M., and Burreson E.M. In vitro propagation of the protozoan Perkinsus marinus, a pathogen of the eastern oyster, Crassostrea virginica. J Eukaryot Microbiol 40 (1993) 304-310
40. La Peyre M.K., Casas S.M., and La Peyre J.F. Salinity effects on three Perkinsus spp. viability, metabolic activity and proliferation. Dis Aquat Organ 71 (2006) 59-74
41. La Peyre J.F., and Chu F.L.E. Simple procedure for the isolation of Perkinsus marinus merozoites, a pathogen of the eastern oyster, Crassostrea virginica. Bull Eur Ass Fish Pathol 14 (1994) 101-103
42. Liu W., and Saint D.A. A new quantitative method of real time reverse transcription polymerase chain reaction assay based on simulation of polymerase chain reaction kinetics. Anal Biochem 302 (2002) 52-59
43. Thellin O., Zorzi W., Lakaye B., De Borma B., Coumans B., Hennen G., et al. Housekeeping genes as internal standards: use and limits. J Biotechnol 75 (1999) 291-295
44. Denz C.R., and Dube D.K. The benefits of 28S rRNA for standardization of reverse transcription-polymerase chain reaction for studying gene expression. Anal Biochem 341 (2005) 382-394
45. Cellura C., Toubiana M., Parrinello N., and Roch P. HSP70 gene expression in Mytilus galloprovincialis hemocytes is triggered by moderate heat shock and Vibrio anguillarum, but not V. splendidus or Micrococcus lysodeikticus. Dev Comp Immunol 30 (2006) 984-997
46. Howard D.W., and Smith C.S. Histological techniques for marine bivalve mollusks. NOAA Technical Memorandum NMFS-F/NEC-25 (1983), US Department of Commerce, Woods Hole, MA
47. Ford S. Range extension by the oyster parasite Perkinsus marinus into the northeastern United States: response to climate change?. J Shellfish Res 15 (1996) 45-56
48. La Peyre M.K., Nickens A.D., Volety A.K., Tolley G.S., and La Peyre J.F. Environmental significance of freshets in reducing Perkinsus marinus infection in eastern oysters Crassostrea virginica: potential management application. Mar Ecol Prog Ser 248 (2003) 165-176
49. Fisher W.S., and Oliver L.M. A whole-oyster procedure for diagnosis of Perkinsus marinus disease using Ray's fluid thioglycollate culture medium. J Shellfish Res 15 (1996) 109-118
50. La Peyre J.F., Smith A.K., and Cooper R.K. Growth inhibition of isolates of the oyster pathogen Perkinsus marinus in vitro with protease inhibitors. In Vitro Cell Dev Biol 33 3-II (1999) 35A
51. Faisal M., La Peyre J.F., Elsayed E., and Wright D.C. Bacitricin inhibits the oyster pathogen Perkinsus marinus in vitro and in vivo. J Aquat Health 11 (1999) 130-138
52. Coombs G.H., and Baxter J. Inhibition of Leishmania amastigote growth by antipain and leupeptin. Ann Trop Med Parasitol 78 (1984) 21-24
53. Franke de Cazzulo B.M., Martinez J., Noth M.J., Coombs G.H., and Cazzulo J.-J. Effects of proteinase inhibitors on the growth and differentiation of Trypanosoma cruzi. FEMS Microbiol 124 (1994) 81-86
54. Rosenthal P.J., Olson J.E., Lee G.K., Palmer J.T., Klaus J.L., and Rasnick D. Antimalarial effects of vinyl sulfone cysteine proteinase inhibitors. Antimicrob Agents Chemother 40 (1996) 1600-1603
55. Engel J.C., Doyle P.S., Hsieh I., and McKerrow J.H. Cysteine protease inhibitors cure and experimental Trypanosoma cruzi infection. J Exp Med 188 (1998) 725-734
56. Shaw M.K., Roos D.S., and Tilney L.G. Cysteine and serine protease inhibitors block intracellular development and disrupt the secretory pathway of Toxoplasma gondii. Microbes Infect 4 (2002) 119-132
57. Xue Q.G., Itoh N., Schey K.L., Cooper R.K., and La Peyre J.F. Evidence indicating the existence of a novel family of serine protease inhibitors that may be involved in marine invertebrate immunity. Fish Shellfish Immunol 27 (2009) 250-259
58. Rosenthal P.J., Lee G.K., and Smith R.E. Inhibition of a Plasmodium vinckei cysteine proteinase cures murine malaria. J Clin Invest 91 (1993) 1052-1056
59. Scory S., Caffrey C.R., Stierhof Y.D., Ruppel A., and Steverding C.R. Trypanosoma brucei: killing of bloodstream forms in vitro and in vivo by the cysteine proteinases inhibitor Z-phe-Ala-CHN2. Exp Parasitol 91 (1999) 327-333
60. Olson J.E., Lee G.K., Semenov A., and Rosenthal P.J. Antimalarial effects in mice of orally administered peptidyl cysteine protease inhibitor. Bioorg Med Chem 7 (1999) 633-638
61. Engel J.C., Doyle P.S., Palmer J., Hsieh I., and Bainton D.F. Cysteine protease inhibitors alter Golgi complex ultrastructure and function in Trypanosoma cruzi. J Cell Sci 111 (1998) 597-606
62. Ford S.E. Effect of repeated hemolymph sampling on growth, mortality, hemolymph protein and parasitism of oysters, Crassostrea virginica. Comp Biochem Physiol Part A 85 (1986) 465-470
63. Fisher W.S., and Newell R.I.E. Seasonal and environmental variation in protein and carbohydrate levels in the hemolymph from American oysters (Crassostrea virginica Gmelin). Comp Biochem Physiol Part A 85 (1986) 365-372
64. Chu F.L.E., and La Peyre J.F. Effect of environmental factors and parasitism on hemolymph lysozyme and protein concentration of American oyster (Crassostrea virginica). J Invertebr Pathol 54 (1989) 224-232
65. Gauthier J.D., and Vasta G.R. Effects of plasma from bivalve mollusk species on the in vitro proliferation of the protistan parasite Perkinsus marinus. J Exp Zool 292 (2002) 221-230
66. Meyers J.E., Burreson E.M., Barber B.J., and Mann R. Susceptibility of diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg, 1793), and eastern oysters, Crassostrea virginica (Gmelin, 1791), to Perkinsus marinus. J Shellfish Res 10 (1991) 433-438
67. Taris N., Lang R.P., Reno P.W., and Camara M.D. Transcriptome response of the Pacific oyster (Crassostrea gigas) to infection with Vibrio tubiashii using cDNA AFLP differential display. Anim Genet (2009) 10.1111/j.1365-2052.20009.01894.x
68. Martin A.W., Harrison F.M., Huston M.I., and Stewart D.M. The blood volumes of some representative mollusks. J Exp Biol 35 (1958) 260-279
69. Thompson R.J., Bayne C.J., Moore M.N., and Carefoot T.H. Hemolymph volume, changes in biochemical composition of blood, and cytological responses of digestive cells in Mytilus californianus Conrad, induced by nutritional, thermal and exposure stress. J Comp Physiol 127 (1978) 287-298
70. Robinson W.W., and Ryan D.K. Transport of cadmium and other metals in the blood of the bivalve mollusk Mercenaria mercenaria. Mar Biol 97 (1988) 101-109
71. La Peyre J.F., Schafhauser D.Y., Rizkalla E.H., and Faisal M. Production of serine proteases by the oyster pathogen Perkinsus marinus (Apicomplexa) in vitro. J Eukaryot Microbiol 42 (1995) 451-458
72. Garreis K.A., La Peyre J.F., and Faisal M. The effects of Perkinsus marinus extracellular products and purified proteases on oyster defense parameters in vitro. Fish Shellfish Immunol 6 (1996) 581-597
73. Faisal M., Schafhauser D.Y., Garreis K.A., Elsayed E., and La Peyre J.F. Isolation and characterization of Perkinsus marinus proteases using bacitracin-sepharose affinity chromatography. Comp Biochem Physiol Part B 123 (1999) 417-426
74. Oliver J.L., Lewis T.D., Faisal M., and Kaattari S.L. Analysis of the effects of Perkinsus marinus proteases on plasma proteins of the eastern oyster (Crassostrea virginica) and the Pacific oyster (Crassostrea gigas). J Invertebr Pathol 74 (1999) 173-183
75. Tall B.D., La Peyre J.F., Bier J.W., Miliotis M.D., Hanes D.E., Kothary M.H., et al. Perkinsus marinus extracellular protease modulates survival of Vibrio vulnificus in eastern oyster (Crassostrea virginica) hemocytes. Appl Environ Microbiol 65 (1999) 4261-4263
76. La Peyre J.F., Yarnall H.A., and Faisal M. Contribution of Perkinsus marinus extracellular products in the infection of eastern oysters (Crassostrea virginica). J Invertebr Pathol 68 (1996) 312-313
77. La Peyre J.F., Chu F.L.E., and Vogelbein W.K. In vitro interaction of Perkinsus marinus with hemocytes of eastern and Pacific oysters. Dev Comp Immunol 19 (1995) 291-304
78. Volety A.K., and Fisher W.S. In vitro killing of Perkinsus marinus by hemocytes of oysters Crasssotrea virginica. J Shellfish Res 19 (2000) 827-834
79. Villamil L., Gomez-Leon J., and Gomez-Chiarri M. Role of nitric oxide in the defenses of Crassostrea virginica to experimental infection with the protozoan parasite Perkinsus marinus. Dev Comp Immunol 31 (2007) 968-977
80. Volety A.K., and Chu F.L.E. Suppression of chemiluminescence of eastern oyster (Crassostrea virginica) hemocytes by the protozoan parasite Perkinsus marinus. Dev Comp Immunol 19 (1999) 135-142
81. Anderson R.S. Perkinsus marinus secretory products modulate superoxide anion production by oyster (Crassostrea virginica) haemocytes. Fish Shellfish Immunol 9 (1998) 51-60
82. Schott E.J., Pecher W.T., Okafor F., and Vasta G.R. The protistan parasite Perkinsus marinus is resistant to selected reactive oxygen species. Exp Parasitol 105 (2003) 232-240