Abstract
Feeding of bacterially encapsulated heat shock proteins (Hsps) to invertebrates is a novel way to limit Vibrio infection. As an example, ingestion of Escherichia coli overproducing prokaryotic Hsps significantly improves survival of gnotobiotically cultured Artemia larvae upon challenge with pathogenic Vibrio campbellii. The relationship between Hsp accumulation and enhanced resistance to infection may involve DnaK, the prokaryotic equivalent to Hsp70, a major molecular chaperone in eukaryotic cells. In support of this proposal, heat-stressed bacterial strains LVS 2 (Bacillus sp.), LVS 3 (Aeromonas hydrophila), LVS 8 (Vibrio sp.), GR 8 (Cytophaga sp.), and GR 10 (Roseobacter sp.) were shown in this work to be more effective than nonheated bacteria in protecting gnotobiotic Artemia larvae against V. campbellii challenge. Immunoprobing of Western blots and quantification by enzyme-linked immunosorbent assay revealed that the amount of DnaK in bacteria and their ability to enhance larval resistance to infection by V. campbellii are correlated. Although the function of DnaK is uncertain, it may improve tolerance to V. campbellii via immune stimulation, a possibility of significance from a fundamental perspective and also because it could be applied in aquaculture, a major method of food production.
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References
Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, Calderwood SK (2000) HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 6:435–442. doi:10.1038/74697
Athman R, Philpott D (2004) Innate immunity via Toll-like receptors and Nod proteins. Curr Opin Microbiol 7:25–32. doi:10.1016/j.mib.2003.12.013
Austin B, Zhang XH (2006) Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol 43:119–124. doi:10.1111/j.1472-765X.2006.01989.x
Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K, Schulte PM, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183. doi:10.1016/S0378-1119(02)00687-X
Bucca G, Brassington AME, Schönfeld HJ, Smith CP (2000) The HspR regulon of Streptomyces coelicolor: a role for the DnaK chaperone as a transcriptional co-repressor. Mol Microbiol 38:1093–1103. doi:10.1046/j.1365-2958.2000.02194.x
Campisi J, Fleshner M (2003) The role of extracellular Hsp72 in acute stress-induced potentiation of innate immunity in physically active rats. J Appl Physiol 94:43–52
Clegg JS, Jackson SA, Hoa NV, Sorgeloos P (2000a) Thermal resistance, developmental rate and heat shock proteins in Artemia franciscana, from San Francisco Bay and Southern Vietnam. J Exp Mar Biol Ecol 252:85–96. doi:10.1016/S0022-0981(00)00239-2
Clegg JS, Jackson SA, Popov VI (2000b) Long-term anoxia in encysted embryos of the crustacean, Artemia franciscana: viability, ultrastructure and stress proteins. Cell Tissue Res 301:433–446. doi:10.1007/s004410000249
de la Vega E, Hall MR, Degnan BM, Wilson KJ (2006) Short-term hyperthermic treatment of Penaeus monodon increases expression of heat shock protein 70 (HSP70) and reduces replication of gill associated virus (GAV). Aquaculture 253:82–90. doi:10.1016/j.aquaculture.2005.07.041
Defoirdt T, Crab R, Wood TK, Sorgeloos P, Verstraete W, Bossier P (2006) Quorum sensing-disrupting brominated furanones protect the gnotobiotic brine shrimp Artemia franciscana from pathogenic Vibrio harveyi, Vibrio campbellii, and Vibrio parahaemolyticus isolates. Appl Environ Microbiol 72:6419–6423. doi:10.1128/AEM.00753-06
Diggles BK, Moss GA, Carson J, Anderson CD (2000) Luminous vibriosis in rock lobster Jasus verreauxi (Decapoda: Palinuridae) phyllosoma larvae associated with infection by Vibrio harveyi. Dis Aquat Org 43:127–137. doi:10.3354/dao043127
Farzanfar A (2006) The use of probiotics in shrimp aquaculture. FEMS Immunol Med Microbiol 48:149–158. doi:10.1111/j.1574-695X.2006.00116.x
Feder ME, Hofmann GE (1999) Heat shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282. doi:10.1146/annurev.physiol.61.1.243
Frankenberg MM, Jackson SA, Clegg JS (2000) The heat shock response of adult Artemia franciscana. J Therm Biol 25:481–490. doi:10.1016/S0306-4565(00)00013-9
Galdiero M, de l'Ero GC, Marcatili A (1997) Cytokine and adhesion molecule expression in human monocytes and endothelial cells stimulated with bacterial heat shock proteins. Infect Immun 65:699–707
Gorospe J, Nakamura K, Abe M, Higashi S (1996) Nutritional contribution of Pseudomonas sp. in Artemia culture. Fish Sci 62:914–918
Hameed A, Balasubramanian G (2000) Antibiotic resistance in bacteria isolated from Artemia nauplii and efficacy of formaldehyde to control bacterial load. Aquaculture 183:195–205. doi:10.1016/S0044-8486(99)00293-8
Hessen D, Andersen T (1990) Bacteria as a source of phosphorous for zooplankton. Hydrobiologia 206:217–223
Jacquier-Sarlin MR, Fuller K, Dinh-Xuan AT, Richard MJ, Polla BS (1994) Protective effects of hsp70 in inflammation. Experientia 50:1031–1038. doi:10.1007/BF01923458
Johnson JD, Fleshner M (2006) Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J Leukoc Biol 79:425–434. doi:10.1189/jlb.0905523
Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685. doi:10.1038/227680a0
MacRae TH (2003) Molecular chaperones, stress resistance and development in Artemia franciscana. Cell Dev Biol 14:251–258. doi:10.1016/j.semcdb.2003.09.019
Marques A, Dhont J, Sorgeloos P, Bossier P (2004a) Evaluation of different yeast cell wall mutants and microalgae strains as feed for gnotobiotically grown brine shrimp Artemia franciscana. J Exp Mar Biol Ecol 321:115–136. doi:10.1016/j.jembe.2004.06.008
Marques A, Francois JM, Dhont J, Bossier P, Sorgeloos P (2004b) Influence of yeast quality on performance of gnotobiotically grown Artemia. J Exp Mar Biol Ecol 310:247–264. doi:10.1016/j.jembe.2004.04.009
Marques A, Dinh T, Ioakeimidis C, Huys G, Swings J, Verstraete W, Dhont J, Sorgeloos P, Bossier P (2005) Effects of bacteria on Artemia franciscana cultured in different gnotobiotic environments. Appl Environ Microbiol 71:4307–4317. doi:10.1128/AEM.71.8.4307-4317.2005
Marques A, Dhont J, Sorgeloos P, Bossier P (2006a) Immunostimulatory nature of β-glucans and baker's yeast in the challenge test of Artemia. Fish Shellfish Immunol 20:682–692. doi:10.1016/j.fsi.2005.08.008
Marques A, Ollevier F, Verstraete W, Sorgeloos P, Bossier P (2006b) Gnotobiotically grown aquatic animals: opportunities to investigate host–microbe interactions. J Appl Microbiol 100:903–918. doi:10.1111/j.1365-2672.2006.02961.x
Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788–3796. doi:10.1101/gad.12.24.3788
Panjwani NN, Popova L, Srivastava PK (2002) Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J Immunol 168:2997–3003
Parsell DA, Lindquist S (1993) The function of heat shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496. doi:10.1146/annurev.ge.27.120193.002253
Pockley AG (2003) Heat shock proteins as regulators of the immune response. Lancet 362:469–476. doi:10.1016/S0140-6736(03)14075-5
Retzlaff C, Yamamoto Y, Hoffman PS, Friedman H, Klein TW (1994) Bacterial heat shock proteins directly induce cytokine mRNA and interleukin-1 secretion in macrophage cultures. Infect Immun 62:5689–5693
Singh V, Aballay A (2006) Heat-shock transcription factor (HSF)-1 pathway required for Caenorhabditis elegans immunity. Proc Natl Acad Sci U S A 103:13092–13097 10.1073/pnas.0604050103
Smith VJ, Brown JH, Hauton C (2003) Immunostimulation in crustaceans: does it really protect against infection? Fish Shellfish Immunol 15:71–90. doi:10.1016/S1050-4648(02)00140-7
Soltanian S, Dhont J, Sorgeloos P, Bossier P (2007) Influence of different yeast cell-wall mutants on performance and protection against pathogenic bacteria (Vibrio campbellii) in gnotobiotically-grown Artemia. Fish Shellfish Immunol 23:141–153. doi:10.1016/j.fsi.2006.09.013
Sorgeloos P, Lavens P, Léger P, Tackaert W, Versichele D (1986) Manual for the culture and use of brine shrimp Artemia in aquaculture. Artemia Reference Center, Faculty of Agriculture, State University of Ghent, Belgium, p 318
Soto-Rodriguez SA, Roque A, Lizarraga-Partida ML, Guerra-Flores AL, Gomez-Gil B (2003) Virulence of luminous vibrios to Artemia franciscana nauplii. Dis Aquat Org 53:231–240. doi:10.3354/dao053231
Sung YY, Van Damme EJM, Sorgeloos P, Bossier P (2007) Non-lethal heat shock protects gnotobiotic Artemia franciscana larvae against virulent Vibrios. Fish Shellfish Immunol 22:318–326. doi:10.1016/j.fsi.2006.05.008
Sung YY, Pineda C, MacRae TH, Sorgeloos P, Bossier P (2008) Exposure of gnotobiotic Artemia franciscana larvae to abiotic stress promotes heat shock protein 70 synthesis and enhances resistance to pathogenic Vibrio campbellii. Cell Stress Chaperones 13:59–66. doi:10.1007/s12192-008-0011-y
Sung YY, Ashame MF, Chen SJ, MacRae TH, Sorgeloos P, Bossier P (2009) Feeding Artemia franciscana (Kellogg) larvae with bacterial heat shock protein, protects from Vibrio campbellii (Baumann) infection. J Fish Dis (in press)
Tinh NTN, Yen VHN, Dierckens K, Sorgeloos P, Bossier P (2008) An acyl homoserine lactone-degrading microbial community improves the survival of first-feeding turbot larvae (Scophthalmus maximus L.). Aquaculture 285:56–62. doi:10.1016/j.aquaculture.2008.08.018
Vadstein O (1997) The use of immunostimulation in marine larviculture: possibilities and challenges. Aquaculture 155:401–17. doi:10.1016/S0044-8486(97)00114-2
Verschuere L, Rombaut G, Huys G, Dhont J, Sorgeloos P, Verstraete W (1999) Microbial control of the culture of Artemia juveniles through pre-emptive colonization by selected bacterial strains. Appl Environ Microbiol 65:2527–2533
Verschuere L, Heang H, Criel G, Sorgeloos P, Verstraete W (2000) Selected bacterial strains protect Artemia sp. from pathogenic effects of Vibrio proteolyticus CW8T2. Appl Environ Microbiol 66:1139–1146. doi:10.1128/AEM.66.3.1139-1146.2000
Yasuda K, Taga N (1980) A mass culture method for Artemia salina using bacteria as food. Mer 18:53–62
Acknowledgements
This work was supported by the University Malaysia Terengganu (UMT, formerly known as University College of Science and Technology Malaysia, KUSTEM) through a doctoral grant to YYS. Research funding was from the Belgian Foundation for Scientific Research (FWO) through the project “Probiont-induced functional responses in aquatic organisms” (no. G.0491.08) and from the Natural Sciences and Engineering Research Council of Canada to THM. We thank Prof. Dr. Bernd Bukau and Dr. Axel Mogk from the Centrum for Molecular Biology, University Heidelberg, Germany for the generous gift of polyclonal antibody to DnaK.
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Sung, Y.Y., Dhaene, T., Defoirdt, T. et al. Ingestion of bacteria overproducing DnaK attenuates Vibrio infection of Artemia franciscana larvae. Cell Stress and Chaperones 14, 603–609 (2009). https://doi.org/10.1007/s12192-009-0112-2
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DOI: https://doi.org/10.1007/s12192-009-0112-2