Characterization of immunomodulatory, anticancer and antioxidant properties of an extracellular polymer produced by Enterococcus sp. in vegetable waste medium
Tóm tắt
This study attempted to evaluate the bioactive properties and characteristics of an extracellular polymer produced by Enterococcus sp. grown in a newly developed vegetable waste media. The vegetable waste medium formulated from corn, garlic, and onion flakes enabled enhanced production of the biopolymer in comparison to other commercially available media. The biopolymer was purified and characterized by Fourier transform infrared spectroscopy (FTIR), scanning electron microscope (SEM), antioxidant ability by hydroxyl, superoxide and di (2, 4, 6 trinitrophenyl) iminoazanium (DPPH) radical scavenging activity. Immunomodulatory and anticancer activities were evaluated by RAW 264.7 and HeLa, respectively. Human Umbilical Vein Endothelial Cells (HUVEC) cell lines were used to determine toxicity to the endothelial system. The molecular mass of the biopolymer was ~ 2 × 105 kDa and it consisted of carbohydrates, uronic acids, hexosamines and proteins. Significant (p < 0.05) production of nitric oxide, tumor necrosis factor (TNF-α), Interleukin-6 (IL-6), IL-ß and antioxidant activity were observed at 100 µg/mL biopolymer concentration. FTIR and SEM analysis revealed a biocompatible, highly porous biopolymer structure with technological suitability. The antioxidant, immunomodulatory and antitumor properties of the Enterococcus sp. biopolymer are likely to have biomedical implications and offer a sustainable approach in terms of de-scaling the production economics while effectively valorizing agro-wastes.
Tài liệu tham khảo
Abdhul K, Ganesh M, Shanmughapriya S, Kanagavel M, Anbarasu K, Natarajaseenivasan K (2014) Antioxidant activity of exopolysaccharide from probiotic strain Enterococcus faecium (BDU7) from Ngari. Int J Biol Macromol 70:450–454
Adebayo-Tayo B, Fashogbon R (2020) In vitro antioxidant, antibacterial, in vivo immunomodulatory, antitumor and hematological potential of exopolysaccharide produced by wild type and mutant Lactobacillus delbureckii subsp bulgaricus. Heliyon 6:03268
Adhikari HS, Yadav PN (2018) Anticancer activity of chitosan, chitosan derivatives, and their mechanism of action. Int J Biomater 2018
Anagnostopoulos DA, Bozoudi D, Tsaltas D (2018) Enterococci isolated from cypriot green table olives as a new source of technological and probiotic properties. Fermentation 4:48
Asker MMS, Sayed OHE, Mahmoud MG, Ramadan MF (2014) Chemical structure and antioxidant activity of a new exopolysaccharide produced from Micrococcus luteus. J Genet Eng Biotechnol 12:121–126
Cambon-Bonavita MA, Raguenes G, Jean J, Vincent P, Guezennec J (2002) A novel polymer produced by a bacterium isolated from a deep sea hydrothermal vent polychaete annelid. J Appl Microbiol 93:310–315
Carswell E, Old LJ, Kassel R, Green S, Fiore N, Williamson B (1975) An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci 72:3666–3670
Chi Z, Zhao S (2003) Optimization of medium and cultivation conditions for pullulan production by a new pullulan-producing yeast strain. Enzyme Microb Technol 33:206–211
Devasagayam T, Tilak J, Boloor K, Sane KS, Ghaskadbi SS, Lele R (2004) Free radicals and antioxidants in human health: current status and future prospects. Japi 52:4
Feghali CA, Wright TM (1997) Cytokines in acute and chronic inflammation. Front Biosci 2:d12–d26
Gutteridge J, Halliwell B (1988) The deoxyribose assay: an assay both for free hydroxyl radical and for site-specific hydroxyl radical production. Biochem J 253:932
Hardia S, Iqbal S (2014) Production of the best natural health supplements using fruit waste materials. Int J Innov Res Dev 3:131–133
Joye IJ, McClements DJ (2014) Biopolymer-based nanoparticles and microparticles: fabrication, characterization, and application. Curr Opin Colloid Interface Sci 19:417–427
Kanemitsu K, Nishino T, Kunishima H, Okamura N, Takemura H, Yamamoto H, Kaku M (2001) Quantitative determination of gelatinase activity among enterococci. J Microbiol Methods 47:11–16. https://doi.org/10.1016/S0167-7012(01)00283-4
Kanmani P, Suganya K, Yuvaraj N, Pattukumar V, Paari K, Arul V (2013) Synthesis and functional characterization of antibiofilm exopolysaccharide produced by Enterococcus faecium MC13 isolated from the gut of fish. Appl Biochem Biotechnol 169:1001–1015
Khaira G, Ganguli A, Ghosh M (2014a) Synthesis and evaluation of antibacterial activity of quaternized biopolymer from Klebsiella terrigena. J Appl Microbiol 116:511–518
Khaira GK, Ganguli A, Ghosh M (2014b) Antimicrobial efficacy and in vivo toxicity studies of a quaternized biopolymeric flocculant. J Water Health 12:656–662
Kieliszek M, Piwowarek K, Kot AM, Pobiega K (2020) The aspects of microbial biomass use in the utilization of selected waste from the agro-food industry. Open Life Sci 15:787–796
Kim Y, Kim SH (2009) Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157: H7. Biochem Biophys Res Commun 379:324–329
Kim HM et al (2019) Biorefining process of carbohydrate feedstock (agricultural onion waste) to acetic acid. ACS Omega 4:22438–22444
Kodali VP, Sen R (2008) Antioxidant and free radical scavenging activities of an exopolysaccharide from a probiotic bacterium. Biotechnol J 3:245–251
Kumar S, Kashyap P (2015) Antiproliferative activity and nitric oxide production of a methanolic extract of Fraxinus micrantha on Michigan Cancer Foundation-7 mammalian breast carcinoma cell line. J Intercult Ethnopharmacol 4:109
Kumar AS, Mody K, Jha B (2007) Evaluation of biosurfactant/bioemulsifier production by a marine bacterium. Bull Environ Contam Toxicol 79:617–621
Lee SY, Lee Y, Wang F (1999) Chiral compounds from bacterial polyesters: sugars to plastics to fine chemicals. Biotechnol Bioeng 65:363–368. https://doi.org/10.1002/(sici)1097-0290(19991105)65:3%3c363::aid-bit15%3e3.0.co;2-1
Liu Y, Tay J-H (2002) The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Res 36:1653–1665
Lobo V, Patil A, Phatak A, Chandra N (2010) Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn Rev 4:118
Majerska J, Michalska A, Figiel A (2019) A review of new directions in managing fruit and vegetable processing by-products. Trends Food Sci Technol 88:207–219
Manero A, Blanch AR (1999) Identification of Enterococcus spp. with a biochemical key. Appl Environ Microbiol 65:4425–4430
Mao R, Tang J, Swanson B (2001) Water holding capacity and microstructure of gellan gels. Carbohydr Polym 46:365–371
Naha PC, Davoren M, Lyng FM, Byrne HJ (2010) Reactive oxygen species (ROS) induced cytokine production and cytotoxicity of PAMAM dendrimers in J774A. 1 cells. Toxicol Appl Pharmacol 246:91–99
Neufeld G, Cohen T, Shraga N, Lange T, Kessler O, Herzog Y (2002) The neuropilins: multifunctional semaphorin and VEGF receptors that modulate axon guidance and angiogenesis. Trends Cardiovasc Med 12:13–19
Pal K, Banthia AK, Majumdar DK (2007) Preparation and characterization of polyvinyl alcohol-gelatin hydrogel membranes for biomedical applications. AAPS PharmSciTech 8:E142–E146
Pan D, Mei X (2010) Antioxidant activity of an exopolysaccharide purified from Lactococcus lactis subsp. lactis 12. Carbohydr Polym 80:908–914
Papadimitriou K et al (2016) Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80:837–890. https://doi.org/10.1128/mmbr.00076-15
Pessione A, Zapponi M, Mandili G, Fattori P, Mangiapane E, Mazzoli R, Pessione E (2014) Enantioselective lactic acid production by an Enterococcus faecium strain showing potential in agro-industrial waste bioconversion: physiological and proteomic studies. J Biotechnol 173:31–40
Popovic N et al (2018) New insight into biofilm formation ability, the presence of virulence genes and probiotic potential of Enterococcus sp dairy isolates. Front Microbiol 9:78
Saadat YR, Khosroushahi AY, Gargari BP (2019) A comprehensive review of anticancer, immunomodulatory and health beneficial effects of the lactic acid bacteria exopolysaccharides. Carbohydr Polym 217:79–89
Shamala T, Vijayendra S, Joshi G (2012) Agro-industrial residues and starch for growth and co-production of polyhydroxyalkanoate copolymer and α-amylase by Bacillus sp. CFR-67. Br J Microbiol 43:1094–1102
Shimada K, Fujikawa K, Yahara K, Nakamura T (1992) Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion. J Agric Food Chem 40:945–948
Singh C, Sharma V, Naik PK, Khandelwal V, Singh H (2011) A green biogenic approach for synthesis of gold and silver nanoparticles using Zingiber officinale Digest. J Nanomater Biostruct 6:535–542
Sohm JA, Edwards BR, Wilson BG, Webb EA (2011) Constitutive extracellular polysaccharide (EPS) production by specific isolates of Crocosphaera watsonii. Front Microbiol 2:229
Song YR, Cha YS (2013) Exopolysaccharide produced by Pediococcus acidilactici M76 isolated from the Korean traditional rice wine, Makgeolli. J Microbiol Biotechnol 23:681–688
Storz P (2005) Reactive oxygen species in tumor progression. Front Biosci 10:1881–1896
Sundaresan M et al (1996) Regulation of reactive-oxygen-species generation in fibroblasts by Rac 1. Biochem J 318:379–382
Suresh Kumar A, Mody K, Jha B (2007) Bacterial exopolysaccharides—a perception. J Basic Microbiol 47:103–117
Tong H et al (2009) Structural characterization and in vitro antitumor activity of a novel polysaccharide isolated from the fruiting bodies of Pleurotus ostreatus. Biores Technol 100:1682–1686
Valledor SJD, Bucheli JEV, Holzapfel WH, Todorov SD (2020) Exploring beneficial properties of the bacteriocinogenic Enterococcus faecium ST10Bz strain isolated from Boza, a Bulgarian cereal-based beverage. Microorganisms 8:1474
Van Meerloo J, Kaspers GJ, Cloos J (2011) Cell sensitivity assays: the MTT assay. Cancer Cell Cult Methods Protocol 237–245
Zhang Q, Li N, Liu X, Zhao Z, Li Z, Xu Z (2004) The structure of a sulfated galactan from Porphyra haitanensis and its in vivo antioxidant activity. Carbohydr Res 339:105–111