Vibrio aestuarianus zinc metalloprotease causes lethality in the Pacific oyster Crassostrea gigas and impairs the host cellular immune defenses

Fish and Shellfish Immunology

Volumn 29, Issue 5, 2010, Pages 753-758

  Labreuche, Yannick ^a   Le Roux, Frédérique ^a,b   Henry, Joël ^c   Zatylny, Céline ^c   Huvet, Arnaud ^a   Lambert, Christophe ^d   Soudant, Philippe ^d   Mazel, Didier ^b   Nicolas, Jean Louis ^a  

^a IFREMER   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE CAEN   (France)

^d INSTITUT UNIVERSITAIRE EUROPÉEN DE LA MER   (France)

Author keywords

Crassostrea gigas; Extracellular products; Hemocytes; Metalloprotease; Oyster; Vibrio aestuarianus

Indexed keywords

CRASSOSTREA GIGAS; OSTREIDAE; VIBRIO; VIBRIO AESTUARIANUS; VIBRIO SPLENDIDUS;

EID: 77956296830     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2010.07.007     Document Type: Article

References (36)

1. Tison D.L., Seidler R.J. Vibrio aestuarianus: a new species from estuarine waters and shellfish. Int J Syst Bacteriol 1983, 33:699-702.
2. Garnier M., Labreuche Y., Garcia C., Robert M., Nicolas J.L. Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microb Ecol 2007, 53:187-196.
3. Garnier M., Labreuche Y., Nicolas J.L. Molecular and phenotypic characterization of Vibrio aestuarianus subsp. francensis subsp. nov., a pathogen of the oyster Crassostrea gigas. Syst Appl Microbiol 2008, 31:358-365.
4. Saulnier D., De Decker S., Haffner P., Cobret L., Robert M., Garcia C. A Large-Scale Epidemiological Study to Identify Bacteria Pathogenic to Pacific Oyster Crassostrea gigas and Correlation Between Virulence and Metalloprotease-like Activity. Microb Ecol 2010, 59(4):787-798.
5. Labreuche Y., Soudant P., Goncalves M., Lambert C., Nicolas J.L. Effects 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.
6. Labreuche Y., Lambert C., Soudant P., Boulo V., Huvet A., Nicolas J.L. Cellular and molecular hemocyte responses of the Pacific oyster, Crassostrea gigas, following bacterial infection with Vibrio aestuarianus strain 01/32. Microbes Infect 2006, 8:2715-2724.
7. Sussman M., Mieog J.C., Doyle J., Victor S., Willis B.L., Bourne D.G. Vibrio zinc metalloprotease causes photoinactivation of coral endosymbionts and coral tissue lesions. PloS One 2009, 4:e4511.
8. Hasegawa H., Gharaibeh D.N., Lind E.J., Häse C.C. Virulence of metalloproteases produced by Vibrio species on Pacific oyster Crassostrea gigas larvae. Dis Aquat Organ 2009, 85:123-131.
9. Nottage A.S., Birkbeck T.H. Purification of a proteinase produced by the bivalve pathogen vibrio alginolyticus ncmb 1339. J Fish Dis 1987, 10.
10. Hasegawa H., Lind E.J., Boin M.A., Häse C.C. The extracellular metalloprotease of Vibrio tubiashii is a major virulence factor for Pacific oyster (Crassostrea gigas) larvae. Appl Environ Microbiol 2008, 74:4101-4110.
11. Le Roux F., Binesse J., Saulnier D., Mazel D. Construction of a Vibrio splendidus Mutant lacking the metalloprotease gene vsm by use of a novel counterselectable suicide vector. Appl Environ Microbiol 2007, 73:777-784.
12. Studier F.W. Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J Mol Biol 1991, 219:37-44.
13. Thompson F.L., Iida T., Swings J. Biodiversity of Vibrios. Microbiol Mol Biol Rev 2004, 68:403-431.
14. Binesse J., Delsert C., Saulnier D., Champomier-Verges M.-C., Zagorec M., Munier-Lehmann H., et al. Metalloprotease vsm is the major Determinant of toxicity for extracellular products of Vibrio splendidus. Appl Environ Microbiol 2008, 74:7108-7117.
15. Sambrook J., Fritsch E.F., Maniatis T. Molecular cloning: a laboratory manual 1989, Cold Spring Harbor, NY. 2nd ed.
16. Matsumoto-Mashimo C., Guerout A.-M., Mazel D. A new family of conditional replicating plasmids and their cognate Escherichia coli host strains. Res Microbiol 2004, 155:455-461.
17. Bernay B., Baudy-Floc'h M., Zanuttini B., Zatylny C., Pouvreau S., Henry J. Ovarian and sperm regulatory peptides regulate ovulation in the oyster Crassostrea gigas. Mol Reprod Dev 2006, 73:607-616.
18. Perlman D., Halvorson H. A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. J Mol Biol 1983, 167:391-409.
19. von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem 1983, 133:17-21.
20. David V.A., Deutch A.H., Sloma A., Pawlyk D., Ally A., Durham D.R. Cloning, sequencing and expression of the gene encoding the extracellular neutral protease, vibriolysin, of Vibrio proteolyticus. Gene 1992, 112:107-112.
21. Milton D.L., Norqvist A., Wolf-Watz H. Cloning of a metalloprotease gene involved in the virulence mechanism of Vibrio anguillarum. J Bacteriol 1992, 174:7235-7244.
22. Vallee B.L., Auld D.S. Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 1990, 29:5647-5659.
23. Rawlings N.D., Barrett A.J. Evolutionary families of metallopeptidases. Meth Enzymol 1995, 248:183-228.
24. Guzman L.M., Belin D., Carson M.J., Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 1995, 177:4121-4130.
25. Johnson C.M., Schleif R.F. In vivo induction kinetics of the arabinose promoters in Escherichia coli. J Bacteriol 1995, 177:3438-3442.
26. Miyada C.G., Stoltzfus L., Wilcox G. Regulation of the araC gene of Escherichia coli: catabolite repression, autoregulation, and effect on araBAD expression. Proc Nat Aca Sci USA 1984, 81:4120-4124.
27. Häse C.C., Finkelstein R.A. Bacterial extracellular zinc-containing metalloproteases. Microbiol Rev 1993, 57:823-837.
28. Miyoshi S.-i., Shinoda S. Microbial metalloproteases and pathogenesis. Microbes Infect 2000, 2:91-98.
29. Varina M., Denkin S.M., Staroscik A.M., Nelson D.R. Identification and characterization of Epp, the secreted processing protease for the Vibrio anguillarum EmpA metalloprotease. J Bacteriol 2008, 190:6589-6597.
30. Sonoda H., Daimon K., Yamaji H., Sugimura A. Efficient production of active Vibrio proteolyticus aminopeptidase in Escherichia coli by co-expression with engineered vibriolysin. Appl Microbiol Biotechnol 2009, 84:191-198.
31. Shinoda S., Miyoshi S.-i., Wakae H., Rahman M., Tomochika K.-i. Bacterial proteases as pathogenic factors, with special emphasis on vibrio proteases. J Toxicol Tox Rev 1996, 15:327-339.
32. Muñoz P., Vance K., Gómez-Chiarri M. Protease activity in the plasma of American oysters, Crassostrea virginica, experimentally infected with the protozoan parasite, Perkinsus marinus. J Parasitol 2003, 89:941-951.
33. Tall B., La Peyre J., Bier J., Miliotis M., Hanes D., Kothary M., et al. Perkinsus marinus extracellular protease modulates survival of Vibrio vulnificus in Eastern oyster (Crassostrea virginica) hemocytes. Appl Environ Microbiol 1999, 65:4261-4263.
34. Garreis K., La Peyre J., Faisal M. The effects of Perkinsus marinus extracellular products and purified proteases on oyster defense parameters in vitro. Fish Shellfish Immunol 1996, 6:581-597.
35. Aktories K., Barbieri J.T. Bacterial cytotoxins: targeting eukaryotic switches. Nat Rev Microbiol 2005, 3:397-410.
36. Raftopoulou M., Hall A. Cell migration: Rho GTPases lead the way. Dev Biol 2004, 265:23-32.