Enhanced resistance against Vibrio harveyi infection by carvacrol and its association with the induction of heat shock protein 72 in gnotobiotic Artemia franciscana

Cell Stress and Chaperones - Tập 22 - Trang 377-387 - 2017
Kartik Baruah1, Parisa Norouzitallab1,2, Ho Phuong Pham Duy Phong1, Guy Smagghe3, Peter Bossier1
1Laboratory of Aquaculture & Artemia Reference Center, Department of Animal Production, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
2Laboratory of Immunology and Animal Biotechnology, Department of Animal Production, Faculty of Bioscience EngineeringGhent University, Ghent, Belgium
3Laboratory of Agrozoology, Department of Crop Protection, Ghent University, Ghent, Belgium

Tóm tắt

Induction of HSP72 is a natural response of stressed organisms that protects against many insults including bacterial diseases in farm (aquatic) animals. It would therefore be of great health benefit to search for natural compounds that are clinically safe yet able to induce HSP72 in animals. The phenolic compound carvacrol, an approved food component, had been shown in in vitro study to act as a co-inducer of HSP72, enhancing HSP72 production only in combination with a bona fide stress compared to the compound alone. However, in vitro model systems do not completely represent an in vivo physiology. Here, using the well-established gnotobiotic Artemia model system, we determined whether carvacrol could induce HSP72 in vivo, whether this putative effect could generate resistance in Artemia against biotic/abiotic stress and also unraveled the mechanism behind the possible HSP72-inducing effect of carvacrol. The gnotobiotic system is crucial for such studies because it avoids the interference of any extraneous factors on host-compound interaction. Here, carvacrol was shown to be a potent HSP72 inducer. Induction of HSP72 was associated with the generation of resistance in Artemia larvae against subsequent lethal heat stress or pathogenic Vibrio harveyi. Our results also provided new insight on the mode of HSP72 inducing action of carvacrol, in which the initial generation of reactive molecule H2O2 by the compound plays a key role. Overall results add new information about the bioactivity of carvacrol and advance our knowledge of this compound as potential prophylactic agent for controlling Vibrio infection in aquaculture animals.

Tài liệu tham khảo

Akagawa M, Shigemitsu T, Suyama K (2003) Production of hydrogen peroxide by polyphenols and polyphenol-rich beverage under quasi physiological conditions. Biosci Biotechnol Biochem 67:2632–2640 Astashkina A, Mann B, Grainger DW (2012) A critical evaluation of in vitro cell culture models for high-throughput drug screening and toxicity. Pharmacol Ther 134:82–106 Austin B, Zhang XH (2006) Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol 43:119–124 Baruah K et al (2009) 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 Baruah K, Ranjan JK, Sorgeloos P, Bossier P (2010) 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 Baruah K, Norouzitallab P, Roberts RJ, Sorgeloos P, Bossier P (2012) A novel heat-shock protein inducer triggers heat shock protein 70 to protect Artemia franciscana against abiotic stressors. Aquacult 334–337:152–158 Baruah K, Norouzitallab P, Shihao L, Sorgeloos P, Bossier P (2013) Feeding truncated heat shock protein 70s protects Artemia franciscana against virulent Vibrio campbellii challenge. Fish Shellfish Immunol 34:183–191 Baruah K, Norouzitallab P, Linayati L, Sorgeloos P, Bossier P (2014) 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 Baruah K et al (2015a) Probing the protective mechanism of poly-ß-hydroxybutyrate against vibriosis by using gnotobiotic Artemia franciscana and Vibrio campbellii as host-pathogen model. Sci Rep 5:9427 Baruah K, Phong HPPD, Norouzitallab P, Defoirdt T (2015b) The gnotobiotic brine shrimp (Artemia franciscana) model system reveals that the phenolic compound pyrogallol protects against infection through its prooxidant activity. Free Radic Biol Med 89:593–601 Boerrigter JG et al (2014) Effects of pro-Tex on zebrafish (Danio rerio) larvae, adult common carp (Cyprinus carpio) and adult yellowtail kingfish (Seriola lalandi). Fish Physiol Biochem 40:1201–1212 Bradford MM (1976) 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 Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods–a review. Int J Food Microbiol 94:223–253 Burt SA et al (2007) Carvacrol induces heat shock protein 60 and inhibits synthesis of flagellin in Escherichia coli O157:H7. Appl Environ Microb 73:4484–4490 Calabrese V, Testa G, Ravagna A, Bates TE, Stella AM (2000) HSP70 induction in the brain following ethanol administration in the rat: regulation by glutathione redox state. Biochem Biophys Res Commun 269:397–400 Chen T, Cao X (2010) Stress for maintaining memory: HSP70 as a mobile messenger for innate and adaptive immunity. Eur J Immunol 40:1541–1544 Chen H, Davidson PM, Zhong Q (2014) Impacts of sample preparation methods on solubility and antilisterial characteristics of essential oil components in milk. Appl Environ Microbiol 80:907–916 Chiu CH, Guu YK, Liu CH, Pan TM, Cheng W (2007) Immune responses and gene expression in white shrimp, Litopenaeus vannamei, induced by Lactobacillus plantarum. Fish Shellfish Immunol 23:364–377 Clegg JS, Jackson SA, Hoa NV, Sorgeloos P (2000) 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 Correia B et al (2013) Is the interplay between epigenetic markers related to the acclimation of cork oak plants to high temperatures? PLoS One 8:e53543 FAO/WHO Committee on Food Additives (2001) Evaluation of certain food additives and contaminants. 55th report. WHO, Geneva FDA (2011) Synthetic flavoring substances and adjuvants. 21CFR 182.60. U.S. Food and Drug Administration, Washington DC Fittipaldi S, Dimauro I, Mercatelli N, Caporossi D (2014) Role of exercise-induced reactive oxygen species in the modulation of heat shock protein response. Free Radic Res 48:52–70 Fridell YW, Sánchez-Blanco A, Silvia BA, Helfand SL (2005) Targeted expression of the human uncoupling protein2 (hUCP2) to adult neuron sex tends life span in the fly. Cell Metab 1:145–152 Huang TC, Lin YT, Chuang KP (2010) Carvacrol has the priming effects of reactive oxygen species (ROS) production in C6 glioma cells. Food Agric Immunol 21:47–55 Iwama GK, Thomas PT, Forsyth RB, Vijayan MM (1998) Heat shock protein expression in fish. Rev Fish Biol Fisheries 8:35–56 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 Kojima K et al (2004) Escherichia coli LPS induces heat shock protein 25 in intestinal epithelial cells through MAP kinase activation. Am J Physiol Gastrointest Liver Physiol 286:G645–G652 Liang WZ et al (2013) The mechanism of carvacrol-evoked [Ca2+]i rises and non-Ca2 + −triggered cell death in OC2 human oral cancer cells. Toxicol 303:152–161 Marques A, Ollevier F, Verstraete W, Sorgeloos P, Bossier P (2006) Gnotobiotically grown aquatic animals: opportunities to investigate host-microbe interactions. J Appl Microbiol 100:903–918 Muralidharan S et al (2014) Moderate alcohol induces stress proteins HSF1 and hsp70 and inhibits proinflammatory cytokines resulting in endotoxin tolerance. J Immunol 193:1975–1987 Nagai Y, Fujikake N, Popiel HA, Wada K (2010) Induction of molecular chaperones as a therapeutic strategy for the polyglutamine diseases. Curr Pharm Biotechnol 11:188–197 Niu Y, Norouzitallab P, Baruah K, Dong S, Bossier P (2014) A plant-based heat shock protein inducing compound modulates host-pathogen interactions between Artemia franciscana and Vibrio campbellii. Aquacult 430:120–127 Norouzitallab P, Baruah K, Dechamma MM, Bossier P (2015) Non-lethal heat shock induces HSP70 and HMGB1 proteins sequentially to protect Artemia franciscana against Vibrio campbellii. Fish Shellfish Immunol 42:395–399 Ohtsuka K, Kawashima D, Gu Y, Saito K (2005) Inducers and coinducers of molecular chaperones. Int J Hyperth 21:703–711 Omar R, Pappolla M (1993) Oxygen free radicals as inducers of heat shock protein synthesis in cultured human neuroblastoma cells: relevance to neurodegenerative disease. Eur Arch Psychiatry Clin Neurosci 242:262–267 Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33:789–801 Sanders BM (1993) Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol 23:49–75 Shoji Y, Nakashims H (2004) Nutraceutics and delivery systems. J Drug Target 12:385–391 Skoula M, Gotsiou P, Naxakis G, Johnson CB (1999) A chemosystematic investigation on the mono- and sesquiterpenoids in the genus Origanum (Labiatae). Phytochemistry 52:649–657 Sung YY, Roberts RJ, Bossier P (2012) Enhancement of Hsp70 synthesis protects common carp Cyprinus carpio L. against lethal ammonia toxicity. J Fish Dis 35:563–568 Tsan MF, Gao B (2009) Heat shock proteins and immune system. J Leukoc Biol 85:905–910 Westerheide SD, Morimoto RI (2005) Heat shock response modulators as therapeutic tools for diseases of protein conformation. J Biol Chem 280:33097–33100 Wieten L et al (2010) A novel heat-shock protein coinducer boosts stress protein Hsp70 to activate T cell regulation of inflammation in autoimmune arthritis. Arthritis Rheum 62:1026–1035 Yan D, Saito K, Ohmi Y, Fujie N, Ohtsuka K (2004) Paeoniflorin, a novel heat shock protein-inducing compound. Cell Stress Chaperon 9:378–389