Influence of ultrasound on Pleurotus pulmonarius (Fr.) Quél. (Grey Oyster Mushroom) – Protective Effects Against Metabolic Syndrome in Rats Fed with a High-fat Diet
DOI:
https://doi.org/10.51200/bijb.v3i.4529Keywords:
cardiovascular, fungal metabolites, green, extraction, ultrasound, mushrooms, natural productsAbstract
The Pleurotus pulmonarius (Fr.) Quel. (Grey Oyster mushroom) is one of the most widely consumed mushroom species worldwide, and it possesses various medicinal properties. The application of ultrasound resulted in P. pulmonarius extracts with improved bioactivities both in cellular and animal models. However, no studies have investigated the preventive effects of ultrasound extract of P. pulmonarius in animal models. In this study, Wistar-Kyoto rats were pre-treated with the ultrasound extract of P. pulmonarius at high (500 mg/kg bw) and low (200 mg/kg bw) doses for 15 days. The rats were subsequently fed with a high-fat diet (HFD) for another 15 days. Rats pre-treated with P. pulmonarius extract from a high-dose ultrasound showed lower levels of serum cholesterol (1.50 mmol/L), triglyceride (0.60 mmol/L), and LDL (0.29 mmol/L). These rats also had lower oxidative stress, with MDA levels of only 10.81 µg/mg protein. The ultrasound extract of P. pulmonarius also exhibited anti-hyperglycaemic effects, whereby rats had lower blood glucose levels. Rats pre-treated with the ultrasound extract of P. pulmonarius also had inhibited inflammatory biomarkers CREB1 (2.85 pmol/mL), NF-κB2 (0.81 ng/mL), and STAT3 (0.48 ng/mL), proving the anti-inflammatory activity of the ultrasound extract. This study is the first to show the ability of P. pulmonarius extract prepared using ultrasound to prevent developing metabolic syndrome such as hyperlipidaemia, hyperglycaemia, oxidative stress, and inflammation in rats fed with HFD.
References
Amirullah, N. A., Zainal Abidin, N., Abdullah, N., & Manickam, S. (2020). Application of ultrasound towards improving the composition of phenolic compounds and enhancing in vitro bioactivities of Pleurotus pulmonarius (Fr.) Quél extracts. Biocatalysis and Agricultural Biotechnology, 31 (C), 101881. https://doi.org/10.1016/j.bcab.2020.101881
Amirullah, N. A., Zainal Abidin, N., Abdullah, N., & Manickam, S. (2021). The ultrasound extract of Pleurotus pulmonarius (Fr.) Quél alleviates metabolic syndromes in hyperlipidaemic Wistar-Kyoto rats fed with a high-fat diet. Biocatalysis and Agricultural Biotechnology, 34 (May), 102019. https://doi.org/10.1016/j.bcab.2021.102019
Aronson, D., & Rayfield, E. J. (2002). How hyperglycemia promotes atherosclerosis: Molecular mechanisms. Cardiovascular Diabetology, 1 (1), 1 – 10. https://doi.org/10.1186/1475-2840-1-1
Awad, T. S., Moharram, H. A., Shaltout, O. E., Asker, D., & Youssef, M. M. (2012). Applications of ultrasound in analysis, processing and quality control of food: A review. Food Research International, 48 (2), 410 – 427. https://doi.org/10.1016/j.foodres.2012.05.004
Ayala, A., Muñoz, M. F., & Argüelles, S. (2014). Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-Hydroxy-2-Nonenal. Oxidative Medicine and Cellular Longevity, 2014, 1 – 31. https://doi.org/10.1155/2014/360438
Balaji, P., Madhanraj, R., Rameshkumar, K., Veeramanikandan, V., Eyini, M., Arun, A., Thulasinathan, B., Al Farraj, D. A., Elshikh, M. S., Alokda, A. M., Mahmoud, A. H., Tack, J. C., & Kim, H. J. (2020). Evaluation of antidiabetic activity of Pleurotus pulmonarius against streptozotocin-nicotinamide induced diabetic wistar albino rats. Saudi Journal of Biological Sciences, 27 (3), 913 – 924. https://doi.org/10.1016/j.sjbs.2020.01.027
Barros, L., Pereira, C., & Ferreira, I. C. F. R. (2013). Optimized analysis of organic acids in edible mushrooms from Portugal by ultra fast liquid chromatography and photodiode array detection. Food Analytical Methods, 6 (1), 309 – 316. https://doi.org/10.1007/s12161-012-9443-1
Björkbacka, H., Kunjathoor, V. V, Moore, K. J., Koehn, S., Ordija, C. M., Lee, M. a, Means, T., Halmen, K., Luster, A. D., Golenbock, D. T., & Freeman, M. W. (2004). Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signalling pathways. Nature Medicine, 10 (4), 416 – 421. https://doi.org/10.1038/nm1008
Boligon, A. A. (2014). Technical evaluation of antioxidant activity. Medicinal Chemistry, 4 (7), 517 – 522. https://doi.org/10.4172/2161-0444.1000188
Carr, A., & Frei, B. (1999). Does vitamin C act as a pro-oxidant under physiological conditions? FASEB Journal : Official Publication of the Federation of American Societies for Experimental Biology, 13 (9), 1007 – 1024. http://www.ncbi.nlm.nih.gov/pubmed/10336883
Dandona, P., Chaudhuri, A., Ghanim, H., & Mohanty, P. (2006). Anti-inflammatory effects of insulin and the pro-inflammatory effects of glucose. Seminars in Thoracic and Cardiovascular Surgery, 18 (4), 293 – 301. https://doi.org/10.1053/j.semtcvs.2006.06.003
Dommermuth, R., & Ewing, K. (2018). Metabolic syndrome. Primary Care: Clinics in Office Practice, 45 (1), 109 – 129. https://doi.org/10.1016/j.pop.2017.10.003
dos Santos Bazanella, G. C., de Souza, D. F., Castoldi, R., Oliveira, R. F., Bracht, A., & Peralta, R. M. (2013). Production of laccase and manganese peroxidase by Pleurotus pulmonarius in solid-state cultures and application in dye decolorization. Folia Microbiologica, 58 (6), 641 – 647. https://doi.org/10.1007/s12223-013-0253-7
Elfirta, R. R., Saskiawan, I., Amalia, R. L. R., Zahrah, A., Ikhwani, N., & Widhyastuti, N. (2023). Kadar karbohidrat dan penapisan senyawa aktif dari Pleurotus pulmonarius yang Diekstraksi menggunakan metode microwave assisted extraction (MAE) dengan beberapa perlakuan suhu [Carbohydrate content and active compound screening of Pleurotus pulmonarius]. Jurnal Biologi Indonesia, 19 (1), 65 – 76. https://doi.org/10.47349/jbi/19012023/65
Flamment, M., Rieusset, J., Vidal, H., Simard, G., Malthièry, Y., Fromenty, B., & Ducluzeau, P. H. (2012). Regulation of hepatic mitochondrial metabolism in response to a high fat diet: A longitudinal study in rats. Journal of Physiology and Biochemistry, 68 (3), 335 – 344. https://doi.org/10.1007/s13105-012-0145-3
Giera, M., Lingeman, H., & Niessen, W. M. A. (2012). Recent advancements in the LC- and GC-based analysis of malondialdehyde (MDA): A brief overview. Chromatographia, 75 (17), 1089 – 1089. https://doi.org/10.1007/s10337-012-2295-4
Gil-Ramírez, A., Smiderle, F. R., Morales, D., Iacomini, M., & Soler-Rivas, C. (2019). Strengths and weaknesses of the aniline-blue method used to test mushroom (1→3)-β-D-glucans obtained by microwave-assisted extractions. Carbohydrate Polymers, 217 (January), 135 – 143. https://doi.org/10.1016/j.carbpol.2019.04.051
GraphPad Prism (5.04). (2010). www.graphpad.com
Grivennikov, S. I., & Karin, M. (2010). Dangerous liaisons: STAT3 and NF-κB collaboration and crosstalk in cancer. Cytokine and Growth Factor Reviews, 21 (1), 11 – 19. https://doi.org/10.1016/j.cytogfr.2009.11.005
Grundy, S. M. (2016). Metabolic syndrome update. Trends in Cardiovascular Medicine, 26 (4), 364 – 373. https://doi.org/10.1016/j.tcm.2015.10.004
Haddad, J. J. (2002). Redox regulation of pro-inflammatory cytokines and IκB-α/NF-κB nuclear translocation and activation. Biochemical and Biophysical Research Communications, 296 (4), 847 – 856. https://doi.org/10.1016/S0006-291X(02)00947-6
Hajer, G. R., van Haeften, T. W., & Visseren, F. L. J. (2008). Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. European Heart Journal, 29 (24), 2959 – 2971. https://doi.org/10.1093/eurheartj/ehn387
Hassan, N. F., Soliman, G. M., Okasha, E. F., & Shalaby, A. M. (2018). Histological, Immunohistochemical, and Biochemical Study of Experimentally Induced Fatty Liver in Adult Male Albino Rat and the Possible Protective Role of Pomegranate. Journal of Microscopy and Ultrastructure, 6 (1), 44 – 55. https://doi.org/10.4103/JMAU.JMAU_5_18
Huang, H. Y., Korivi, M., Yang, H. T., Huang, C. C., Chaing, Y. Y., & Tsai, Y. C. (2014). Effect of Pleurotus tuber-regium polysaccharides supplementation on the progression of diabetes complications in obese-diabetic rats. The Chinese Journal of Physiology, 57 (4), 198 – 208. https://doi.org/10.4077/CJP.2014.BAC245
Huang, J., Wu, Q., Lin, Z., Liu, S., Su, Q., & Pan, Y. (2020). Therapeutic effects of chitin from Pleurotus Eryngii on high-fat diet induced obesity in rats. Acta Scientiarum Polonorum, Technologia Alimentaria, 19 (3), 279 – 289. https://doi.org/10.17306/J.AFS.0775
Jeong, S. C., Jeong, Y. T., Yang, B. K., Islam, R., Koyyalamudi, S. R., Pang, G., Cho, K. Y., & Song, C. H. (2010). White button mushroom (Agaricus bisporus) lowers blood glucose and cholesterol levels in diabetic and hypercholesterolemic rats. Nutrition Research, 30 (1), 49 – 56. https://doi.org/10.1016/j.nutres.2009.12.003
Kakimoto, P. A., & Kowaltowski, A. J. (2016). Effects of high fat diets on rodent liver bioenergetics and oxidative imbalance. Redox Biology, 8, 216 – 225. https://doi.org/10.1016/j.redox.2016.01.009
Karin, M., Cao, Y., Greten, F. R., & Li, Z. W. (2002). NF-κB in cancer: from innocent bystander to major culprit. Nature Reviews Cancer, 2 (4), 301 – 310. https://doi.org/10.1038/nrc780
Kroes, B. H., van den Berg, A. J., Quarles van Ufford, H. C., van Dijk, H., Labadie, R. P., Vandenberg, A. J. J., Vanufford, H. C. Q., Vandijk, H., & Labadie, R. P. (1992). Anti-inflammatory activity of gallic acid. Planta Medica, 58 (6), 499 – 504. https://doi.org/10.1055/s-2006-961535
Lavi, I., Levinson, D., Peri, I., Nimri, L., Hadar, Y., & Schwartz, B. (2010). Orally administered glucans from the edible mushroom Pleurotus pulmonarius reduce acute inflammation in dextran sulfate sodium-induced experimental colitis. British Journal of Nutrition, 103 (3), 393 – 402. https://doi.org/10.1017/S0007114509991760
Lefkowitch, J. (2020). Scheuer’s liver biopsy interpretation (10th Edition). Elsevier.
Masella, R., Santangelo, C., D’Archivio, M., LiVolti, G., Giovannini, C., & Galvano, F. (2012). Protocatechuic acid and human disease prevention: biological activities and molecular mechanisms. Current Medicinal Chemistry, 19, 2901 – 2917. https://doi.org/10.2174/092986712800672102
Milovanovic, I., Zengin, G., Maksimovic, S., & Tadic, V. (2021). Supercritical and ultrasound‐assisted extracts from Pleurotus pulmonarius mushroom: chemical profiles, antioxidative, and enzyme‐inhibitory properties. Journal of the Science of Food and Agriculture, 101 (6), 2284 – 2293. https://doi.org/10.1002/jsfa.10849
Nair, J., Ghatge, M., Kakkar, V. V., & Shanker, J. (2014). Network analysis of inflammatory genes and their transcriptional regulators in coronary artery disease. PloS One, 9 (4), 1 – 12. https://doi.org/10.1371/journal.pone.0094328
Nguyen, T. K., Im, K. H., Choi, J., Shin, P. G., & Lee, T. S. (2016). Evaluation of antioxidant, anti-cholinesterase, and anti-inflammatory effects of culinary mushroom Pleurotus pulmonarius. Mycobiology, 444 (4), 291 – 301.
Pamukcu, B., Lip, G. Y. H., & Shantsila, E. (2011). The NF-κB pathway in atherosclerosis: a potential therapeutic target for atherothrombotic vascular disease. Thrombosis Research, 128 (2), 117 – 123. https://doi.org/10.1016/j.thromres.2011.03.025
Petrie, J. R., Guzik, T. J., & Touyz, R. M. (2018). Diabetes, hypertension, and cardiovascular disease: Clinical insights and vascular mechanisms. Canadian Journal of Cardiology, 34 (5), 575 – 584. https://doi.org/10.1016/j.cjca.2017.12.005
Podszun, M. C., Grebenstein, N., Spruss, A., Schlueter, T., Kremoser, C., Bergheim, I., & Frank, J. (2014). Dietary α-tocopherol and atorvastatin reduce high-fat-induced lipid accumulation and down-regulate CD36 protein in the liver of guinea pigs. The Journal of Nutritional Biochemistry, 25 (5), 573 – 579. https://doi.org/10.1016/j.jnutbio.2014.01.008
Qi, L., Saberi, M., Zmuda, E., Wang, Y., Altarejos, J., Zhang, X., Dentin, R., Hedrick, S., Bandyopadhyay, G., Hai, T., Olefsky, J., & Montminy, M. (2009). Adipocyte CREB Promotes Insulin Resistance in Obesity. Cell Metabolism, 9 (3), 277 – 286. https://doi.org/10.1016/j.cmet.2009.01.006
R Development Core Team (2008). Computational many-particle physics. In H. Fehske, R. Schneider, & A. Weiße (Eds.), R Foundation for Statistical Computing (Vol. 739, Issue 2.11.1). Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-540-74686-7
Ragunathan, R., Gurusamy, R., Palaniswamy, M., & Swaminathan, K. (1996). Cultivation of Pleurotus spp. on various agro-residues. Food Chemistry, 55 (2), 139 – 144. https://doi.org/10.1016/0308-8146(95)00079-8
Rahman, M. A., Abdullah, N., & Aminudin, N. (2014). Inhibitory effect on in vitro LDL oxidation and HMG Co-a reductase activity of the liquid-liquid partitioned fractions of Hericium erinaceus (Bull.) persoon (Lion’s Mane Mushroom). BioMed Research International, 2014, 1 – 9. https://doi.org/10.1155/2014/828149
Rajamäki, K., Lappalainen, J., Öörni, K., Välimäki, E., Matikainen, S., Kovanen, P. T., & Eklund, K. K. (2010). Cholesterol Crystals Activate the NLRP3 Inflammasome in Human Macrophages: A Novel Link between Cholesterol Metabolism and Inflammation. PLoS ONE, 5 (7), 1 – 9. https://doi.org/10.1371/journal.pone.0011765
Razali, F. N., Sinniah, S. K., Hussin, H., Zainal Abidin, N., & Shuib, A. S. (2016). Tumor suppression effect of Solanum nigrum polysaccharide fraction on Breast cancer via immunomodulation. International Journal of Biological Macromolecules, 92, 185 – 193. https://doi.org/10.1016/j.ijbiomac.2016.06.079
Razzaghi-Asl, N., Garrido, J., Khazraei, H., Borges, F., & Firuzi, O. (2013). Antioxidant properties of hydroxycinnamic acids: A review of structure- activity relationships. Current Medicinal Chemistry, 20 (36), 4436 – 4450. http://www.ncbi.nlm.nih.gov/pubmed/23834166
Reckless, J. P. D., & Lawrence, J. M. (2003). Hyperlipidemia (Hyperlipidaemia). In Encyclopedia of Food Sciences and Nutrition (pp. 3183 – 3192). https://doi.org/10.1016/B0-12-227055-X/00613-1
Ro, H. S., Kim, S. S., Ryu, J. S., Jeon, C. O., Lee, T. S., & Lee, H. S. (2007). Comparative studies on the diversity of the edible mushroom Pleurotus eryngii: ITS sequence analysis, RAPD fingerprinting, and physiological characteristics. Mycological Research, 111 (6), 710 – 715. https://doi.org/10.1016/j.mycres.2007.03.016
Ruiz, P., Perlina, A., Mumtaz, M., & Fowler, B. A. (2016). A systems biology approach reveals converging molecular mechanisms that link different POPs to common metabolic diseases. Environmental Health Perspectives, 124 (7), 1034 – 1041. https://doi.org/10.1289/ehp.1510308
Sperling, L. S., Mechanick, J. I., Neeland, I. J., Herrick, C. J., Després, J. P., Ndumele, C. E., Vijayaraghavan, K., Handelsman, Y., Puckrein, G. A., Araneta, M. R. G., Blum, Q. K., Collins, K. K., Cook, S., Dhurandhar, N. V., Dixon, D. L., Egan, B. M., Ferdinand, D. P., Herman, L. M., Hessen, S. E., … Grundy, S. M. (2015). The CardioMetabolic Health Alliance. Journal of the American College of Cardiology, 66 (9), 1050 – 1067. https://doi.org/10.1016/j.jacc.2015.06.1328
Steinberg, D. (2009). The LDL modification hypothesis of atherogenesis: An update. Journal of Lipid Research, 50 (Supplement), S376 – S381. https://doi.org/10.1194/jlr.R800087-JLR200
Sukkar, S. G., & Rossi, E. (2004). Oxidative stress and nutritional prevention in autoimmune rheumatic diseases. Autoimmunity Reviews, 3 (3), 199 – 206. https://doi.org/10.1016/j.autrev.2003.09.002
Tak, P. P., & Firestein, G. S. (2001). NF-κB: A key role in inflammatory diseases. Journal of Clinical Investigation, 107 (1), 7 – 11. https://doi.org/10.1172/JCI11830
Tao, Y., Han, Y., Liu, W., Peng, L., Wang, Y., Kadam, S., Show, P. L., & Ye, X. (2019). Parametric and phenomenological studies about ultrasound-enhanced biosorption of phenolics from fruit pomace extract by waste yeast. Ultrasonics Sonochemistry, 52 (August 2018), 193 – 204. https://doi.org/10.1016/j.ultsonch.2018.11.018
Test No. 425: Acute Oral Toxicity: Up-and-Down Procedure. (2008). In Organisation for Economic Co-operation and Development. OECD Publishing. https://doi.org/10.1787/9789264071049-en
Thompson, L. U., Yoon, J. H., Jenkins, D. J. A., Wolever, T. M. S., & Jenkins, A. L. (1984). Relationship between polyphenol intake and blood glucose response of normal and diabetic individuals. The American Journal of Clinical Nutrition, 39 (5), 745 – 751. https://doi.org/10.1093/ajcn/39.5.745
Tung, Y. T., Pan, C. H., Chien, Y. W., & Huang, H. Y. (2020). Edible mushrooms: Novel medicinal agents to combat metabolic syndrome and associated diseases. Current Pharmaceutical Design, 26 (39), 4970 – 4981. https://doi.org/10.2174/1381612826666200831151316
Van Gaal, L. F., Mertens, I. L., & De Block, C. E. (2006). Mechanisms linking obesity with cardiovascular disease. Nature, 444 (7121), 875 – 880. https://doi.org/10.1038/nature05487
Velika, B., & Kron, I. (2012). Antioxidant properties of benzoic acid derivatives against superoxide radical. Free Radicals and Antioxidants, 2 (4), 62 – 67. https://doi.org/10.5530/ax.2012.4.11
Vinatoru, M., Mason, T. J., & Calinescu, I. (2017). Ultrasonically assisted extraction (UAE) and microwave assisted extraction (MAE) of functional compounds from plant materials. TrAC - Trends in Analytical Chemistry, 97, 159 – 178. https://doi.org/10.1016/j.trac.2017.09.002
Wang, H. H., Lee, D. K., Liu, M., Portincasa, P., & Wang, D. Q. H. (2020). Novel insights into the pathogenesis and management of the metabolic syndrome. Pediatric Gastroenterology, Hepatology and Nutrition, 23 (3), 180 – 230. https://doi.org/10.5223/PGHN.2020.23.3.189
Wen, A. Y., Sakamoto, K. M., & Miller, L. S. (2010). The role of the transcription factor CREB in immune function. The Journal of Immunology, 185 (11), 6413 – 6419. https://doi.org/10.4049/jimmunol.1001829
Xu, H., Li, X., Adams, H., Kubena, K., & Guo, S. (2019). Etiology of metabolic syndrome and dietary intervention. International Journal of Molecular Sciences, 20 (1), 1 – 19. https://doi.org/10.3390/ijms20010128
Yildiz, S., Yildiz, Ü. C., Gezer, E. D., & Temiz, A. (2002). Some lignocellulosic wastes used as raw material in cultivation of the Pleurotus ostreatus culture mushroom. Process Biochemistry, 38 (3), 301 – 306. https://doi.org/10.1016/S0032-9592(02)00040-7
Zainal Abidin, M. H., Abdullah, N., & Zainal Abidin, N. (2016a). Protective effect of antioxidant extracts from grey oyster mushroom, Pleurotus pulmonarius (Agaricomycetes), against human low-density lipoprotein oxidation and aortic endothelial cell damage. International Journal of Medicinal Mushrooms, 18 (2), 109 – 121. https://doi.org/10.1615/IntJMedMushrooms.v18.i2.20
Zainal Abidin, M. H., Abdullah, N., & Zainal Abidin, N. (2016b). Therapeutic Properties of Pleurotus species (Oyster mushrooms) for Atherosclerosis: A Review. International Journal of Food Properties, 10942912.2016.1210162. https://doi.org/10.1080/10942912.2016.1210162
Zainal Abidin, M. H., Abdullah, N., & Zainal Abidin, N. (2018). Antiatherogenic potential of extracts from the gray oyster medicinal mushroom, Pleurotus pulmonarius (agaricomycetes), In Vitro. International Journal of Medicinal Mushrooms, 20 (3), 283 – 290. https://doi.org/10.1615/IntJMedMushrooms.2018025821
Downloads
Published
How to Cite
Issue
Section
Total Views: 93
| 
Total Downloads: 29
