Browse > Article
http://dx.doi.org/10.5352/JLS.2021.31.2.183

Immunomodulatory Effects of Euglena gracilis Extracts  

Yu, Sun Nyoung (Department of Microbiology and Immunology, Pusan National University School of Medicine)
Park, Bo Bae (Department of Microbiology and Immunology, Pusan National University School of Medicine)
Kim, Ji Won (Department of Microbiology and Immunology, Pusan National University School of Medicine)
Hwang, You Lim (Department of Microbiology and Immunology, Pusan National University School of Medicine)
Kim, Sang Hun (Section of Pulmonary, Critical Care and Sleep Medicine, Department of Internal Medicine, Yale University School of Medicine)
Kim, Sunah (Department of Civil and Environmental Engineering, Pusan National University)
Lee, Taeho (Department of Civil and Environmental Engineering, Pusan National University)
Ahn, Soon Cheol (Department of Microbiology and Immunology, Pusan National University School of Medicine)
Publication Information
Journal of Life Science / v.31, no.2, 2021 , pp. 183-191 More about this Journal
Abstract
Euglena gracilis is a microalga of great biotechnological interest that can create high levels of bioactive compounds, such as tocopherol, paramylon, and folic acid. The objective of this study was to investigate the biological activities of extracts from E. gracilis, especially those focused on immunological activity. E. gracilis biomass was extracted with hot water (HWE) and the remaining pellet was continuously extracted with methanol (HWME). First, we examined the effect of two extracts from E. gracilis on the production of nitric oxide (NO) and the expression of pro-inflammation cytokines, including IL-1β, IL-6, and TNF-α in murine macrophage RAW 264.7 cells. HWE treatment dose-dependently increased the production of IL-1β and TNF-α. On the other hand, treatment with HWME significantly decreased the generation of NO and pro-inflammatory cytokines (IL-6 and TNF-α) in lipopolysaccharide (LPS)-stimulated macrophage cells. In addition, other biological activities of the extracts were further analyzed: α-glucosidase inhibition, protein tyrosine phosphatase (PTP1B) inhibition, tyrosinase inhibition, xanthine oxidase (XO) inhibition, and angiotensin-converting enzyme (ACE) inhibition. Analysis of these biological activities showed that HWE has more inhibitory effects than HWME against α-glucosidase, tyrosinase, and XO agents. However, the inhibition of PTP1B and ACE with HWME were higher than with HWE. Taken together, the results suggested that E. gracilis possesses various biological activities―especially immunological capabilities―through regulation of cytokine production. Therefore, E. gracilis extract may be potentially useful for food material with immune-regulating effects.
Keywords
Biological activity; Euglena gracilis; immunomodulatory activity; nitric oxide; pro-inflammatory cytokines;
Citations & Related Records
연도 인용수 순위
  • Reference
1 An, H. J., Rim, H. K., Jeong, H. J., Hong, S. H., Um, J. Y. and Kim, H. M. 2010. Hot water extracts of Chlorella vulgaris improve immune function in protein-deficient weanling mice and immune cells. Immunopharmacol. Immunotoxicol. 32, 585-592.   DOI
2 Bogdan, C. 2015. Nitric oxide synthase in innate and adaptive immunity: an update. Trends Immunol. 36, 161-178.   DOI
3 Bohlen, H. J. 2015. Nitric oxide and the cardiovascular system. Compr. Physiol. 5, 808-823.   DOI
4 Caroprese, M., Albenzio, M., Ciliberti, M. G., Francavilla, M. and Sevi, A. 2012. A mixture of phytosterols from Dunaliella tertiolecta affects proliferation of peripheral blood mononuclear cells and cytokine production in sheep. Vet. Immunol. Immunopathol. 150, 27-35.   DOI
5 Chaplin, D. D. 2010. Overview of the immune response. J. Allergy Clin. Immunol. 125, S3-23.   DOI
6 Do, J., Gwak, J., Rho, J. J., Lee, K. and Ki, D. C. 2019. Inhibitory effect of medicinal plant extracts on xanthine oxidase activity. J. Appl. Biol. Chem. 62, 275-280.   DOI
7 Evans, M., Falcone, P. H., Crowley, D. C., Sulley, A. M., Campbell, M., Zakaria, N., Lasrado, J. A., Fritz, E. P. and Herrlinger, K. A. 2019. Effect of a Euglena gracilis fermentate on immune function in healthy, active adults: a randomized, double-blind, placebo-controlled trial. Nutrients 11, 2926.   DOI
8 Feghali, C. A. and Wright, T. M. 1997. Cytokines in acute and chronic inflammation. Front. Biosci. 2, d12-26.   DOI
9 Finamore, F., Palmery, M., Bensehaila, S. and Peluso, I. 2017. Antioxidant, immunomodulating, and microbial-modulating activities of the sustainable and ecofriendly spirulina. Oxid. Med. Cell Longev. 2017, 3247528.   DOI
10 Habte-Tsion, H., Kolimadu, G. D., Rossi Jr, W. and Filer, K. 2020. Effects of Schizochytrium and micro-minerals on immune, antioxidant, inflammatory and lipid-metabolism status of Micropterus salmoides fed high- and low-fishmeal diets. Sci. Rep. 10, 7457.   DOI
11 Iwasaki, A. and Medzhitov, R. 2015. Control of adaptive immunity by the innate immune system. Nat. Immunol. 16, 343-353.   DOI
12 Koizumi, N., Sakagami, H., Utsumi, A., Fujinaga, S., Takeda, M., Asano, K., Sugawara, I., Ichikawa, S., Kondo, H. and Mori, S. 1993. Anti-HIV (human immunodeficiency virus) activity of sulfated paramylon. Antiviral Res. 21, 1-14.   DOI
13 Jung, S. H. and Park, J. K. 2014. Isolation and characterization of bioactive substances from microalgae. J. Chitin. Chitosan 19, 100-106.
14 Kany, S., Vollrath, J. T. and Relja, B. 2019. Cytokines in inflammatory disease. Int. J. Mol. Sci. 20, 6008.   DOI
15 Kim, H. M., Oh, H., Jeong, J. H., Lee, S. C., Moon, H. J. and Jeong, Y. S. 2017. Functional evaluation of marine micro-algae Amphidinium carterae extract. Kor. J. Food Preserv. 24, 673-679.   DOI
16 Lee, W. S., Choi, A., Ahn, C. Y., Oh, H., Ahn, J. S. and Oh, H. M. 2004. Screening of bioactive materials from freshwater microalgae. Algae 9, 271-276.
17 McComb, S., Thiriot, A., Akache, B., Krishnan, L. and Stark, F. 2019. Introduction to the immune system. Methods Mol. Biol. 2024, 1-24.   DOI
18 Palm, N. W., de Zoete, M. R. and Flavell, R. A. 2015. Immune-microbiota interactions in health and disease. Clin. Immunol. 159, 122-127.   DOI
19 Pujiastuti, D. Y., Amin, M. N. G., Alamsjah, M. A. and Hsu, J. L. 2019. Marine organisms as potential sources of bioactive peptides that inhibit the activity of angiotensin I-converting enzyme: a review. Molecules 24, 2541.   DOI
20 Phillips, F. C., Jensen, G. S., Showman, L., Tonda, R., Horst, G. and Levine, R. 2019. Particulate and solubilized β-glucan and non-β-glucan fractions of Euglena gracilis induce proand anti-inflammatory innate immune cell responses and exhibit antioxidant properties. J. Inflamm. Res. 12, 49-64.   DOI
21 Radak, Z., Naito, H. and Taylor, A. W. 2012. Is it the cause of muscle soreness? Nitric Oxide 26, 89-94.   DOI
22 Stefano, G. B. and Kream, R. M. 2011. Reciprocal regulation of cellular nitric oxide formation by nitric oxide synthase and nitrite reductases. Med. Sci. Monit. 17, RA221-6.   DOI
23 Russo, R., Barsanti, L., Evangelista, V., Frassanito, A. M., Longo, V., Pucci, L., Penno, G. and Gualtieri, P. 2016. Euglena gracilis paramylon activates human lymphocytes by upregulating pro-inflammatory factors. Food Sci. Nutr. 5, 205-214.
24 Silva, S. C., Ferreira, I. C. F. R., Dias, M. M. and Barreiro, F. 2020. Microalgae-derived pigments: a 10-year bibliometric review and industry and market trend analysis. Molecules 25, 3406.   DOI
25 Soares, A. T., de Costa, D. C., Vieira, A. A. H. and Filho, N. R. A. 2019. Analysis of major carotenoids and fatty acid composition of freshwater microalgae. Heliyon 5, e01529.   DOI
26 Wang, X., Wang, H., Pierre, J. F., Wang, S., Huang, H., Zhang, J., Liang, S., Zeng, O., Zhang, C., Huang, M., Ruan, C., Lin, J. and Li, H. 2018. Marine microalgae bioengineered Schizochytrium sp. meal hydrolysates inhibits acute inflammation. Sci. Rep. 8, 9848.   DOI
27 Sugiyama, A., Suzuki, K., Mitra, S., Arashida, R., Yoshida, E., Nakano, R., Yabuta, Y. and Takeuchi, T. 2009. Hepatoprotective effects of paramylon, a beta-1, 3-D-glucan isolated from Euglena gracilis Z, on acute liver injury induced by carbon tetrachloride in rats. J. Vet. Med. Sci. 71, 885-890.   DOI
28 Suh, S. S., Hong, J. M., Kim, E. J., Jung, S. W., Kim, S. M., Kim, J. E., Kim, I. C. and Kim, S. 2018. Anti-inflammation and anti-cancer activity of ethanol extract of antarctic freshwater microalga, Micractinium sp. Int. J. Med. Sci. 15, 929-936.   DOI
29 Tossavainen, M., Ilyass, U., Ollilainen, V., Valkonen, K., Ojala, A. and Romantschuk, M. 2019. Influence of long term nitrogen limitation on lipid, protein and pigment production of Euglena gracilis in photoheterotrophic cultures. PeerJ. 7, e6624.   DOI
30 Yasuda, K., Ogushi, M., Nakashima, A., Nakano, Y. and Suzuki, K. 2018. Accelerated wound healing on the skin using a film dressing with β-glucan paramylon. In Vivo 32, 799-805.   DOI
31 Zaharudin, N., Staerk, D. and Dragsted, L. O. 2019. Inhibition of α-glucosidase activity by selected edible seaweeds and fucoxanthin. Food Chem. 270, 481-486.   DOI
32 Weigert, A., von Knethen, A., Fuhrmann, D., Dehne, N. and Brune, B. 2018. Redox-signals and macrophage biology. Mol. Aspects Med. 63, 70-87.   DOI
33 Watanabe, T., Shimada, R., Matsuyama, A., Yuasa, M., Sawamura, H., Yoshida, E. and Suzuki, K. 2013. Antitumor activity of the β-glucan paramylon from Euglena against preneoplastic colonic aberrant crypt foci in mice. Food Funct. 4, 1685-1690.   DOI