[en] Psidium guajava L. is known to possess immune-modulatory properties in humans and other mammals. Although the positive effects of P. guajava-based diets on the immunological status have been shown for some fish species, the underlying molecular mechanisms of its protective effects remain to be investigated. The aims of this study were to evaluate the immune-modulatory effects of two guava fractions from dichloromethane (CC) and ethyl acetate (EA) on striped catfish with in vitro and in vivo experiments. Striped catfish head kidney leukocytes were stimulated with 40, 20, 10 and 0 μg/ml of each extract fraction, and the immune parameters (ROS, NOS, and lysozyme) were examined at 6 and 24 h post stimulation. A final concentration of each fraction at 40, 10 and 0 μg/fish was then intraperitoneally injected into the fish. After 6, 24, and 72 h of administration, immune parameters as well as the expression of some cytokines related to innate and adaptive immune responses, inflammation, and apoptosis were measured in the head kidney. Results indicated that the humoral (lysozyme) and cellular (ROS and NOS) immune endpoints were regulated differently by CC and EA fractions depending on dose and time in both, in vitro and in vivo experiments. With regards to the in vivo experiment, the CC fraction of the guava extract could significantly enhance the TLRs-MyD88-NF-κB signaling pathway by upregulating its cytokine genes (tlr1, tlr4, myd88, and traf6), following the upregulation of inflammatory (nfκb, tnf, il1β, and il6) and apoptosis (tp53 and casp8) genes 6 h after injection. Moreover, fish treated with both CC and EA fractions significantly enhanced cytokine gene expression including lys and inos at the later time points - 24 h or 72 h. Our observations suggest that P. guajava fractions modulate the immune, inflammatory, and apoptotic pathways.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Nhu, Truong Quynh; College of Agriculture, Cantho University, Campus II, Cantho City, Viet Nam. Electronic address: tqnhu@ctu.edu.vn
Hang, Bui Thi Bich; College of Aquaculture and Fisheries, Cantho University, Campus II, Cantho City, Viet Nam. Electronic address: btbhang@ctu.edu.vn
Huong, Do Thi Thanh ; College of Aquaculture and Fisheries, Cantho University, Campus II, Cantho City, Viet Nam. Electronic address: dtthuong@ctu.edu.vn
Scippo, Marie-Louise ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
Phuong, Nguyen Thanh ; College of Aquaculture and Fisheries, Cantho University, Campus II, Cantho City, Viet Nam. Electronic address: ntphuong@ctu.edu.vn
Quetin-Leclercq, Joëlle; Louvain Drug research Institute (LDRI) Pharmacognosy Research group, Université catholique de Louvain, B-1200, Brussels, Belgium. Electronic address: joelle.leclercq@uclouvain.be
Kestemont, Patrick ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA) ; Research Unit in Environmental and Evolutionary Biology (URBE), Institute of Life, Earth and Environment (ILEE), University of Namur, Rue de Bruxelles 61, B-5000, Namur, Belgium. Electronic address: Belgium.patrick.kestemont@unamur.be
Language :
English
Title :
Psidium guajava L.- dichloromethane and ethyl acetate fractions ameliorate striped catfish (Pangasianodon hypophthalmus) status via immune response, inflammatory, and apoptosis pathways.
The experiments were supported by the Commission of Cooperation and Development of the Académie de Recherche et d’Enseignement Supérieur (ARES-CCD) and the General Directorate for Cooperation and Development (DGD) in Belgium through the AquaBioActive Research Project for Development between the University of Namur , the University of Liège and the Université Catholique de Louvain in Belgium , and the Can Tho University in Vietnam .The experiments were supported by the Commission of Cooperation and Development of the Académie de Recherche et d'Enseignement Supérieur (ARES-CCD) and the General Directorate for Cooperation and Development (DGD) in Belgium through the AquaBioActive Research Project for Development between the University of Namur, the University of Liège and the Université Catholique de Louvain in Belgium, and the Can Tho University in Vietnam. The authors thank Prof. Bui Thi Buu Hue and Dr. Le Thi Bach for the supply of the plant fractions used in this study. We are very grateful to Dr. Carolin Mayer (ILEE scientific manager) for her revision of the English syntax.
Díaz-de-Cerio, E., Verardo, V., Gómez-Caravaca, A.M., Fernández-Gutiérrez, A., Segura-Carretero, A., Health Effects of Psidium guajava L. Leaves: an overview of the last decade. Int. J. Mol. Sci., 18(4), 2017, 897, 10.3390/ijms18040897 PMID: 28441777; PMCID: PMC5412476.
Gutiérrez, R.M.P., Mitchell, S., Solis, R.V., Psidium guajava: a review of its traditional uses, phytochemistry and pharmacology. J. Ethnopharmacol. 117:1 (2008), 1–27, 10.1016/j.jep.2018.12.001 PMID: 30639057. (Accessed 10 January 2019)
Naseer, S., Hussain, S., Naeem, N., Pervaiz, M., Rahman, M., The phytochemistry and medicinal value of Psidium guajava (guava). Clinical Phytoscience, 4(1), 2018, 32, 10.1186/s40816-018-0093-8.
García-Betanzos, C.I., Hernández-Sánchez, H., Bernal-Couoh, T.F., Quintanar-Guerrero, D., Zambrano-Zaragoza, M.d.l.L., Physicochemical, total phenols and pectin methylesterase changes on quality maintenance on guava fruit (Psidium guajava L.) coated with candeuba wax solid lipid nanoparticles-xanthan gum. Food Res. Int. 101 (2017), 218–227, 10.1016/j.foodres.2017.08.065.
Arain, A., Hussain Sherazi, S.T., Mahesar, S.A., Sirajuddin, Essential oil from Psidium guajava leaves: an excellent source of β-Caryophyllene. Nat. Prod. Commun., 14(5), 2019, 1934578X19843007, 10.1177/1934578X19843007.
Tella, T., Masola, B., Mukaratirwa, S., The effect of Psidium guajava aqueous leaf extract on liver glycogen enzymes, hormone sensitive lipase and serum lipid profile in diabetic rats. Biomed. Pharmacother. 109 (2019), 2441–2446, 10.1080/14786419.2019.1648462.
Giri, S.S., Sen, S.S., Chi, C., Kim, H.J., Yun, S., Park, S.C., Sukumaran, V., Effect of guava leaves on the growth performance and cytokine gene expression of Labeo rohita and its susceptibility to Aeromonas hydrophila infection. Fish Shellfish Immunol. 46:2 (2015), 217–224, 10.1016/j.fsi.2015.05.051.
Hoseinifar, S.H., Sohrabi, A., Paknejad, H., Jafari, V., Paolucci, M., Van Doan, H., Enrichment of common carp (Cyprinus carpio) fingerlings diet with Psidium guajava: the effects on cutaneous mucosal and serum immune parameters and immune related genes expression. Fish Shellfish Immunol. 86 (2019), 688–694, 10.1016/j.fsi.2018.12.001.
Choi, S.Y., Hwang, J.H., Park, S.Y., Jin, Y.J., Ko, H.C., Moon, S.W., Kim, S.J., Fermented guava leaf extract inhibits LPS-induced COX-2 and iNOS expression in Mouse macrophage cells by inhibition of transcription factor NF-κB. Phytother Res. 22:8 (2008), 1030–1034, 10.1002/ptr.2419.
Sen, S.S., Sukumaran, V., Giri, S.S., Park, S.C., Flavonoid fraction of guava leaf extract attenuates lipopolysaccharide-induced inflammatory response via blocking of NF-κB signalling pathway in Labeo rohita macrophages. Fish Shellfish Immunol. 47:1 (2015), 85–92, 10.1016/j.fsi.2015.08.031.
Mbaveng, A.T., Manekeng, H.T., Nguenang, G.S., Dzotam, J.K., Kuete, V., Efferth, T., Cytotoxicity of 18 Cameroonian medicinal plants against drug sensitive and multi-factorial drug resistant cancer cells. J. Ethnopharmacol. 222 (2018), 21–33, 10.1016/j.jep.2018.04.036.
Hoseinifar, S.H., Sohrabi, A., Paknejad, H., Jafari, V., Paolucci, M., Van Doan, H., Enrichment of common carp (Cyprinus carpio) fingerlings diet with Psidium guajava: the effects on cutaneous mucosal and serum immune parameters and immune related genes expression. Fish Shellfish Immunol. 86 (2019), 688–694, 10.1016/j.fsi.2018.12.001.
Nhu, T.Q., Dam, N.P., Hang, B.T.B., Hue, B.T.B., Scippo, M.-L., Phuong, N.T., Quetin-Leclercq, J., Kestemont, P., Immunomodulatory potential of extracts, fractions and pure compounds from Phyllanthus amarus and Psidium guajava on striped catfish (Pangasianodon hypophthalmus) head kidney leukocytes. Fish Shellfish Immunol. 104 (2020), 289–303, 10.1016/j.fsi.2020.05.051.
Nhu, T.Q., Bich Hang, B.T., Vinikas, A., Bach, L.T., Buu Hue, B.T., Thanh Huong, D.T., Quetin-Leclercq, J., Scippo, M.-L., Phuong, N.T., Kestemont, P., Screening of immuno-modulatory potential of different herbal plant extracts using striped catfish (Pangasianodon hypophthalmus) leukocyte-based in vitro tests. Fish Shellfish Immunol. 93 (2019), 296–307, 10.1016/j.fsi.2019.07.064.
Boyum, A., Separation of leukocytes from blood and bone marrow. Scand. J. Clin. Lab. Invest. 21 (1968), 97–105.
Pierrard, M.-A., Roland, K., Kestemont, P., Dieu, M., Raes, M., Silvestre, F., Fish peripheral blood mononuclear cells preparation for future monitoring applications. Anal. Biochem. 426:2 (2012), 153–165, 10.1016/j.ab.2012.04.009.
Ellis, A., Stolen, J.S., Fletcher, T.C., Anderson, D.P., Robertson, B.S., Van Muiswinkel, W.B., (eds.) Lysozyme Assays–In: Techniques in Fish Immunology, 1, 1990, SOS Publications, Fair Haven, USA.
Milla, S., Mathieu, C., Wang, N., Lambert, S., Nadzialek, S., Massart, S., Henrotte, E., Douxfils, J., Mélard, C., Mandiki, S., Spleen immune status is affected after acute handling stress but not regulated by cortisol in Eurasian perch, Perca fluviatilis. Fish Shellfish Immunol. 28:5–6 (2010), 931–941, 10.1016/j.fsi.2010.02.012.
Rook, G., Steele, J., Umar, S., Dockrell, H., A simple method for the solubilisation of reduced NBT, and its use as a colorimetric assay for activation of human macrophages by γ-interferon. J. Immunol. Methods 82:1 (1985), 161–167, 10.1016/0022-1759(85)90235-2.
Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res., 29(9), 2001, 10.1093/nar/29.9.e45 e45-e45.
Van Hai, N., The use of medicinal plants as immunostimulants in aquaculture: a review. Aquaculture 446 (2015), 88–96, 10.1016/j.aquaculture.2015.03.014.
Truong, D.-H., Nguyen, D.H., Ta, N.T.A., Bui, A.V., Do, T.H., Nguyen, H.C., Evaluation of the use of different solvents for phytochemical constituents, antioxidants, and in vitro anti-inflammatory activities of severinia buxifolia. J. Food Qual., 2019, 2019, 10.1155/2019/8178294.
Oghogho, O., Nimenibo-Uadia, R., Phytochemical screening, GC-MS analysis and in vitro inhibition of alpha-amylase and alpha-glucosidase activities by methanol extract of Psidium guajava leaves and fractions. J. Pharmacogn. Phytochem. 8:5 (2019), 634–640.
Hall, A.M., Baskiyar, S., Heck, K.L., Hayden, M.D., Ren, C., Nguyen, C., Seals, C.D., Monu, E., Calderón, A.I., Investigation of the chemical composition of antibacterial Psidium guajava extract and partitions against foodborne pathogens. Food Chem., 403, 2023, 134400, 10.1016/j.foodchem.2022.134400.
Grayfer, L., Kerimoglu, B., Yaparla, A., Hodgkinson, J.W., Xie, J., Belosevic, M., Mechanisms of fish macrophage antimicrobial immunity. Front. Immunol., 9, 2018, 10.3389/fimmu.2018.01105.
Atakisi, E., Merhan, O., Nitric Oxide Synthase and Nitric Oxide Involvement in Different Toxicities, Nitric Oxide Synthase: Simple Enzyme-Complex Roles. 2017, 197.
Nguyen, V.T., Ko, S.C., Oh, G.W., Heo, S.Y., Jung, W.K., Effects of psidium guajava leaf extract on apoptosis induction through mitochondrial dysfunction in HepG2 cells. Kor. J. Microbiol. Biotechnol. 47:1 (2019), 43–53, 10.4014/mbl.1806.06001.
Arancibia-Radich, J., González-Blázquez, R., Alcalá, M., Martín-Ramos, M., Viana, M., Arribas, S., Delporte, C., Fernández-Alfonso, M.S., Somoza, B., Gil-Ortega, M., Beneficial effects of murtilla extract and madecassic acid on insulin sensitivity and endothelial function in a model of diet-induced obesity. Sci. Rep., 9(1), 2019, 10.1038/s41598-018-36555-1.
Holderness, J., Hedges, J.F., Daughenbaugh, K., Kimmel, E., Graff, J., Freedman, B., Jutila, M.A., Response of γδ T cells to plant-derived tannins. Crit. Rev. Immunol., 28(5), 2008, 10.1615/critrevimmunol.v28.i5.20.
Kolodziej, H., Kiderlen, A.F., Antileishmanial activity and immune modulatory effects of tannins and related compounds on Leishmania parasitised RAW 264.7 cells. Phytochemistry 66:17 (2005), 2056–2071, 10.1016/j.phytochem.2005.01.011.
Fletcher, T.C., White, A., Lysozyme activity in the plaice (Pleuronectes platessa L.). Cell. Mol. Life Sci. 29:10 (1973), 1283–1285, 10.1007/BF01935119.
Yu, H., Chen, J., Liu, S., Zhang, A., Xu, X., Wang, X., Lu, P., Cheng, G., Large-scale production of functional human lysozyme in transgenic cloned goats. J. Biotechnol. 168:4 (2013), 676–683, 10.1016/j.jbiotec.2013.10.023.
El-Ahmady, S.H., Ashour, M.L., Wink, M., Chemical composition and anti-inflammatory activity of the essential oils of Psidium guajava fruits and leaves. J. Essent. Oil Res. 25:6 (2013), 475–481, 10.1080/10412905.2013.796498.
Jash, C., Kumar, G.S., Binding of alkaloids berberine, palmatine and coralyne to lysozyme: a combined structural and thermodynamic study. RSC Adv. 4:24 (2014), 12514–12525, 10.1039/C3RA46053C.
Takeda, K., Akira, S., Toll-like receptors in innate immunity. Int. Immunol. 17:1 (2005), 1–14, 10.1038/35100529.
Chen, Y., Li, H., Li, M., Niu, S., Wang, J., Shao, H., Li, T., Wang, H., Salvia miltiorrhiza polysaccharide activates T Lymphocytes of cancer patients through activation of TLRs mediated -MAPK and -NF-κB signaling pathways. J. Ethnopharmacol. 200 (2017), 165–173, 10.1016/j.jep.2017.02.029.
Su, J., Dong, J., Huang, T., Zhang, R., Yang, C., Heng, J., Myeloid differentiation factor 88 gene is involved in antiviral immunity in grass carp Ctenopharyngodon idella. J. Fish. Biol. 78:3 (2011), 973–979, 10.1111/j.1095-8649.2011.02910.x.
Chi, C., Giri, S.S., Jun, J.W., Kim, H.J., Yun, S., Kim, S.G., Park, S.C., Immunomodulatory Effects of a bioactive compound isolated from Dryopteris crassirhizoma on the grass carp Ctenopharyngodon idella. J. Immun. Res., 2016, 2016, 10, 10.1155/2016/3068913.
Lawrence, T., The nuclear factor NF-κB pathway in inflammation. Cold Spring Harbor Perspect. Biol., 1(6), 2009, a001651, 10.1101/cshperspect.a001651.
Khatua, S., Acharya, K., Alkali treated antioxidative crude polysaccharide from Russula alatoreticula potentiates murine macrophages by tunning TLR/NF-κB pathway. Sci. Rep., 9(1), 2019, 1713, 10.1038/s41598-018-37998-2.
Shen, T., Wang, G., You, L., Zhang, L., Ren, H., Hu, W., Qiang, Q., Wang, X., Ji, L., Gu, Z., Polysaccharide from wheat bran induces cytokine expression via the toll-like receptor 4-mediated p38 MAPK signaling pathway and prevents cyclophosphamide-induced immunosuppression in mice. Food Nutr. Res., 61(1), 2017, 1344523, 10.1080/16546628.2017.1344523.
El Mansouri, F.E., Chabane, N., Zayed, N., Kapoor, M., Benderdour, M., Martel-Pelletier, J., Pelletier, J.P., Duval, N., Fahmi, H., Contribution of H3K4 methylation by SET-1A to interleukin-1–induced cyclooxygenase 2 and inducible nitric oxide synthase expression in human osteoarthritis chondrocytes. Arthritis Rheum. 63:1 (2011), 168–179, 10.1002/art.27762.
Palmqvist, P., Lundberg, P., Lundgren, I., Hänström, L., Lerner, U., IL-1β and TNF-α regulate IL-6-type cytokines in gingival fibroblasts. J. Dent. Res. 87:6 (2008), 558–563, 10.1177/154405910808700614.
Behar, S., Martin, C., Booty, M., Nishimura, T., Zhao, X., Gan, H., Divangahi, M., Remold, H., Apoptosis is an innate defense function of macrophages against. Mycobacterium tuberculosis, Mucosal immunology 4:3 (2011), 279–287, 10.1038/mi.2011.3.
Milutinović, M.G., Maksimović, V.M., Cvetković, D.M., Nikodijević, D.D., Stanković, M.S., Pešić, M., Marković, S.D., Potential of Teucrium chamaedrys L. to modulate apoptosis and biotransformation in colorectal carcinoma cells. J. Ethnopharmacol., 240, 2019, 111951, 10.1016/j.jep.2019.111951.
Liu, J., Uematsu, H., Tsuchida, N., Ikeda, M.-A., Essential role of caspase-8 in p53/p73-dependent apoptosis induced by etoposide in head and neck carcinoma cells. Mol. Cancer, 10(1), 2011, 95, 10.1186/1476-4598-10-95.