Probing the protective mechanism of poly-ß-hydroxybutyrate against vibriosis by using gnotobiotic Artemia franciscana and Vibrio campbellii as host-pathogen model

Scientific Reports - Tập 5 Số 1
Kartik Baruah1, Tran T. Huy1, Parisa Norouzitallab1, Yufeng Niu1, Sanjay Gupta2, Peter De Schryver1, Peter Bossier1
1Lab of Aquaculture &Artemia Reference Center, Department of Animal Production, Faculty of Bioscience Engineering, Ghent University, Rozier 44, Gent 9000, Belgium.
2Directorate of Cold Water Fisheries Research, Chhirapani Field Centre, Champawat, Uttarakhand 262523, India.

Tóm tắt

AbstractThe compound poly-ß-hydroxybutyrate (PHB), a polymer of the short chain fatty acid ß-hydroxybutyrate, was shown to protect experimental animals against a variety of bacterial diseases, (including vibriosis in farmed aquatic animals), albeit through undefined mechanisms. Here we aimed at unraveling the underlying mechanism behind the protective effect of PHB against bacterial disease using gnotobiotically-cultured brine shrimp Artemia franciscana and pathogenic Vibrio campbellii as host-pathogen model. The gnotobiotic model system is crucial for such studies because it eliminates any possible microbial interference (naturally present in any type of aquatic environment) in these mechanistic studies and furthermore facilitates the interpretation of the results in terms of a cause effect relationship. We showed clear evidences indicating that PHB conferred protection to Artemia host against V. campbellii by a mechanism of inducing heat shock protein (Hsp) 70. Additionally, our results also showed that this salutary effect of PHB was associated with the generation of protective innate immune responses, especially the prophenoloxidase and transglutaminase immune systems – phenomena possibly mediated by PHB-induced Hsp70. From overall results, we conclude that PHB induces Hsp70 and this induced Hsp70 might contribute in part to the protection of Artemia against pathogenic V. campbellii.

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Tài liệu tham khảo

Nicolas, J. L., Gatesoupe, F. J., Froueli, S., Bachere, E. & Gueguen, Y. What alternatives to antibiotics are conceivable for aquaculture? Prod. Anim. 20, 253–258 (2007).

Sapkota, A. et al. Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ. Int. 34, 1215–1226 (2008).

Defoirdt, T., Boon, N., Sorgeloos, P., Verstraete, W. & Bossier, P. Short-chain fatty acids and poly-β-hydroxyalkanoates: (New) Biocontrol agents for a sustainable animal production. Biotechnol. Adv. 27, 680–685 (2009).

von Engelhardt, W., Bartels, J., Kirschberger, S., Meyer zu Düttingdorf, H. D. & Busche, R. Role of short-chain fatty acids in the hind gut. Vet. Q. 20, 52–59 (1998).

Cherrington, C. A., Hinton, M., Pearson, G. R. & Chopra, I. Short-chain organic acids at pH 5.0 kill Escherichia-coli and Salmonella spp without causing membrane perturbation. J. Appl. Bacteriol. 70, 161–165 (1991).

Defoirdt, T., Halet, D., Sorgeloos, P., Bossier, P. & Verstraete, W. Short-chain fatty acids protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. Aquacult. 261, 804–808 (2006).

Defoirdt, T. et al. The bacterial storage compound poly-beta-hydroxybutyrate protects Artemia franciscana from pathogenic Vibrio campbellii. Environ. Microbiol. 9, 445–452 (2007).

Halet, D. et al. Poly-beta-hydroxybutyrate-accumulating bacteria protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. FEMS Microbiol. Ecol. 60, 363–369 (2007).

Ren, H. et al. Short-chain fatty acids induce intestinal epithelial heat shock protein 25 expression in rats and IEC 18 cells. Gastroenterology 121, 631–639 (2001).

Hishiya, A. & Takayama, S. Molecular chaperones as regulators of cell death. Oncogene 27, 6489–6506 (2008).

Tutar, L. & Tutar, Y. Heat shock proteins: an overview. Curr. Pharm. Biotechnol. 11, 216–222 (2010).

Johnson, J. D. & Fleshner, M. Releasing signals, secretory pathways and immune function of endogenous extracellular heat shock protein 72. J. Leukoc. Biol. 79, 425–434 (2006).

Tsan, M. F. & Gao, B. Heat shock proteins and immune system. J. Leukoc. Biol. 85, 905–910 (2009).

Chen, T. & Cao, X. Stress for maintaining memory: HSP70 as a mobile messenger for innate and adaptive immunity. Eur. J. Immunol. 40, 1541–1544 (2010).

Baruah, K., Norouzitallab, P., Linayati, L., Sorgeloos, P. & Bossier, P. Reactive oxygen species generated by a heat shock protein (Hsp) inducing product contributes to Hsp70 production and Hsp70-mediated protective immunity in Artemia franciscana against pathogenic vibrios. Dev. Comp. Immunol. 46, 470–479 (2014).

Baruah, K., Ranjan, J. K., Sorgeloos, P. & Bossier, P. Efficacy of homologous and heterologous heat shock protein 70s as protective agents to gnotobiotic Artemia franciscana challenged with Vibrio campbellii. Fish. Shellfish. Immunol. 29, 733–739 (2010).

Baruah, K., Ranjan, J., Sorgeloos, P., MacRae, T. H. & Bossier, P. Priming the prophenoloxidase system of Artemia franciscana by heat shock proteins protects against Vibrio campbellii challenge. Fish. Shellfish. Immunol. 31, 134–141 (2011).

Ryckaert, J. et al. Heat shock proteins protect platyfish (Xiphophorus maculatus) from Yersinia ruckeri induced mortality. Fish. Shellfish. Immunol. 28, 228–231 (2010).

Sung, Y. Y., Van Damme, E. J. M., Sorgeloos, P. & Bossier, P. Non-lethal heat shock protects gnotobiotic Artemia franciscana larvae against virulent vibrios. Fish. Shellfish. Immunol. 22, 318–326 (2007).

Baruah, K., Norouzitallab, P., Shihao, L., Sorgeloos, P. & Bossier, P. Feeding truncated heat shock protein 70s protect Artemia franciscana against virulent Vibrio campbellii challenge. Fish. Shellfish. Immunol. 34, 183–191 (2013).

Thai, T. Q. et al. Poly-ß-hydroxybutyrate content and dose of the bacterial carrier for Artemia enrichment determine the performance of giant freshwater prawn larvae. Appl. Microbiol. Biotechnol. 98, 5205–5215 (2014).

Fernández, R. G. Artemia bioencapsulation I. Effect of particle sizes on the filtering behavior of Artemia franciscana. J. Crustacean. Biol. 21, 435–442 (2001).

Parhar, K., Baer, K. A., Parker, K. & Ropeleski, M. J. Short-chain fatty acid mediated phosphorylation of heat shock protein 25: effects on camptothecin-induced apoptosis. Am. J. Physiol. Gastrointest. Liver. Physiol. 291, G178–G188 (2006).

Vogel, C. & Marcotte, E. M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13, 227–232 (2012).

De Maio, A. Heat shock proteins. Facts, thoughts and dreams. Shock 11, 1–12 (1999).

Theodorakis, N. G., Drujan, D. & De Maio, A. Thermotolerant cells show an attenuated expression of Hsp70 after heat shock. J. Biol. Chem. 274, 12081–12086 (1999).

Li, D. & Duncan, R. F. Transient acquired thermotolerance in Drosophila, correlated with rapid degradation of Hsp7O during recovery. Eur. J. Biochem. 231, 454–465 (1995).

Arvans, D. L. et al. Luminal bacterial flora determines physiological expression of intestinal epithelial cytoprotective heat shock proteins 25 and 72. Am. J. Physiol. Gastrointest. Liver. Physiol. 288, G696–G704 (2005).

Hu, B., Phuoc, L. H., Sorgeloos, P. & Bossier, P. Bacterial HSP70 (DnaK) is an efficient immune stimulator in Litopenaeus vannamei. Aquacult. 418–419, 87–93 (2014).

Cerenius, L. & Söderhäll, K. The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198, 116–126 (2004).

Jiravanichpaisal, P., Lee, B. L. & Söderhäll, K. Cell-mediated immunity in arthropods: Hematopoiesis, coagulation, melanization and opsonization. Immunobiol. 211, 213–236 (2006).

Cerenius, L., Lee, B. L. & Söderhäll, K. The proPO system: pros and cons for its role in invertebrate immunity. Trends. Immunol. 29, 263–271 (2008).

Gao, H., Li, F., Dong, B., Zhang, O. & Xiang, J. Molecular cloning and characterisation of prophenoloxidase (proPO) cDNA from Fenneropenaeus chinensis and its transcription injected by Vibrio anguillarum. Mol. Biol. Rep. 36, 1159–1166 (2009).

Cerenius, L. & Söderhäll, K. Coagulation in invertebrates. J. Innate. Immunol. 3, 3–8 (2011).

Chen, M.-Y., Hu, K.-Y., Huang, C.-C. & Song, Y.-L. More than one type of transglutaminase in invertebrates? A second type of transglutaminase is involved in shrimp coagulation. Dev. Comp. Immunol. 29, 1003–1016 (2005).

Lin, X., Söderhäll, K. & Söderhäll, I. Transglutaminase activity in the hematopoietic tissue of a crustacean, Pacifastacus leniusculus, importance in hemocyte homeostasis. BMC. Immunol. 9, 58 (2008).

Babu, D. T., Antony, S. P., Joseph, S. P., Bright, A. R. & Philip, R. Marine yeast Candida aquaetextoris S527 as a potential immunostimulant in black tiger shrimp Penaeus monodon. J. Invertebrate. Pathol. 112, 243–252 (2013).

Ganz, T. Iron in innate immunity: starve the invaders. Curr. Opin. Immunol. 21, 63–67. (2009).

Ong, S. T., Ho, J. Z. S., Hoc, B. & Ding, J. L. Iron-withholding strategy in innate immunity. Immunobiology 211, 295–314 (2006).

Weinberg, E. D. Iron availability and infection. Biochim. Biophys. Acta. 1790, 600–605 (2009).

Wischmeyer, P. E., Musch, M. W., Madonna, M. B., Thisted, R. & Chang, E. B. Glutamine protects intestinal epithelial cells: role of inducible HSP70. Am. J. Physiol. Gastrointest. Liver. Physiol. 272, G879–G884 (1997).

Baruah, K. et al. In vivo effects of single or combined N-acyl homoserine lactone quorum sensing signals on the performance of Macrobrachium rosenbergii larvae. Aquacult. 288, 233–238 (2009).

Baruah, K., Norouzitallab, P., Roberts, R. J., Sorgeloos, P. & Bossier, P. A novel heat-shock protein inducer triggers heat shock protein 70 to protect Artemia franciscana against abiotic stressors. Aquacult 334–337, 152–158 (2012).

Clegg, J. S., Jackson, S. A., Hoa, N. V. & Sorgeloos, P. 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 (2000).

Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).

Pfaffl, M. W., Horgan, G. W. & Dempfle, L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of the relative expression results in real-time PCR. Nucleic. Acids. Res. 30, 1–10 (2002).

Ashida, M., Ishizaki, Y. & Iwahana, H. Activation of prophenoloxidase by bacterial cell walls or b-l,3 glucans in plasma of the silkworm Bombyx mori. Biochem. Biophys. Res. Commun. 113, 562–568 (1983).

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