RESEARCH PAPER
The anticancer activity of laccase from white rot fungus Cerrena unicolor on the example of its action on Caov-3 and NIH:OVCAR-3 ovarian cancer cells
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1
Department of Human Physiology of the Chair of Preclinical Sciences, Medical University, Lublin, Poland
2
Student Research Group/ Department of Human Physiology of the Chair of Preclinical Sciences, Medical University, Lublin, Poland
3
Department of Biochemistry and Biotechnology, Institute of Biological Sciences, Maria Curie-Skłodowska University, Lublin, Poland
Corresponding author
Dominika Pigoń-Zając
Department of Human Physiology of the Chair of Preclinical Sciences, Medical University of Lublin, Radziwiłłowska 11, 20-080, Lublin, Poland
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ABSTRACT
Introduction and objective:
According to epidemiological data, ovarian cancer is diagnosed in 240,000 women per year, which is why it is the seventh most common cancer among women worldwide. In addition, among gynaecological cancers it is characterized by the highest mortality. However, there is still no effective treatment, which is why maintenance therapies have a decisive impact on the quality of life of patients. Cerrena unicolor is an example of a medical fungus that produces a laccase enzyme (LAC), as well as synthesizing low-molecular secondary metabolites with a wide spectrum of biological activity. LAC, as demonstrated previously, shows cytotoxic and anti-side activity against cancer cells. The aim of the study was to assess the anti-cancer properties of the extract from the mushroom Cerrena unicolor against ovarian cancer cells.
Material and methods:
The study was carried out on two cellular lines of ovarian cancer: NIH:OVCAR-3 and Caov-3, differing in sensitivity to platinum compounds. In the first stage of the study, the values of the concentration of Cerrena unicolor extract were determined, at which point growth and proliferation were inhibited without a cytotoxic effect in the tested cell lines. For this purpose, classic MTT and BrdU tests were used. The second stage of the study consisted in examining the impact of the preparation on the proliferative and migration potential of cancer cells, using the ECIS system.
Results:
The study showed that the examined laccase showed cytotoxic and antiproliferative effect on the cells of the tested cancer lines.
Conclusions:
Following previous and current studies on Cerrena unicolor, extracts obtained from this fungus can be safely used in anticancer therapy or chemoprevention with no significant harmful effects on normal cells.
ACKNOWLEDGEMENTS
The study was financed from State budget funds allocated by the Minister of Education and Science via the ‘Student scientific clubs create innovations programme’(Agreement No. SKN/SP/570640/2023).
REFERENCES (34)
1.
Webb PM, Jordan SJ. Epidemiology of epithelial ovarian cancer. Best Pract Res Clin Obstet Gynaecol. 2017;41:3–14. doi:10.1016/j.bpobgyn.2016.08.006.
2.
Kuroki L, Guntupalli SR. Treatment of epithelial ovarian cancer. BMJ. 2020;371:m3773. doi:10.1136/bmj.m3773.
3.
Ali AT, Al-Ani O, Al-Ani F. Epidemiology and risk factors for ovarian cancer. Prz menopauzalny = Menopause Rev. 2023;22(2):93–104. doi:10.5114/pm.2023.128661.
4.
Kossaï M, Leary A, Scoazec J-Y, Genestie C. Ovarian Cancer: A Heterogeneous Disease. Pathobiology. 2018;85(1–2):41–49. doi:10.1159/000479006.
5.
Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71(3):209–249. doi:10.3322/caac.21660.
6.
Zhang R, Siu MKY, Ngan HYS, Chan KKL. Molecular Biomarkers for the Early Detection of Ovarian Cancer. Int J Mol Sci. 2022;23(19). doi:10.3390/ijms231912041.
7.
Stewart C, Ralyea C, Lockwood S. Ovarian Cancer: An Integrated Review. Semin Oncol Nurs. 2019;35(2):151–156. doi:10.1016/j.soncn.2019.02.001.
8.
Pięt M, Zając A, Paduch R, et al. Chemopreventive activity of bioactive fungal fractions isolated from milk-supplemented cultures of Cerrena unicolor and Pycnoporus sanguineus on colon cancer cells. 3 Biotech. 2021;11(1):1–13. doi:10.1007/s13205-020-02591-w.
9.
Matuszewska A, Karp M, Jaszek M, et al. Laccase purified from Cerrena unicolor exerts antitumor activity against leukemic cells. Oncol Lett. 2016;11(3):2009–2018. doi:10.3892/ol.2016.4220.
10.
Matuszewska A, Jaszek M, Stefaniuk D, Ciszewski T, Matuszewski Ł. Anticancer, antioxidant, and antibacterial activities of low molecular weight bioactive subfractions isolated from cultures of wood degrading fungus Cerrena unicolor. PLoS One. 2018;13(6):e0197044. doi:10.1371/journal.pone.0197044.
11.
Stefaniuk D, Misztal T, Pięt M, et al. Thromboelastometric analysis of anticancer cerrena unicolor subfractions reveal their potential as fibrin glue drug carrier enhancers. Biomolecules. 2021;11(9). doi:10.3390/biom11091263.
12.
Patel S, Goyal A. Recent developments in mushrooms as anti-cancer therapeutics: a review. 3 Biotech. 2012;2(1):1–15. doi:10.1007/s13205-011-0036-2.
13.
Rashid S, Unyayar A, Mazmanci MA, McKeown SR, Banat IM, Worthington J. A study of anti-cancer effects of Funalia trogii in vitro and in vivo. Food Chem Toxicol. 2011;49(7):1477–1483. doi:
https://doi.org/10.1016/j.fct.....
14.
Janusz G, Rogalski J, Szczodrak J. Increased production of laccase by Cerrena unicolor in submerged liquid cultures. World J Microbiol Biotechnol. 2007;23(10):1459–1464. doi:10.1007/s11274-007-9390-y.
15.
Zhang G-Q, Tian T, Liu Y-P, Wang H-X, Chen Q-J. A laccase with anti-proliferative activity against tumor cells from a white root fungus Abortiporus biennis. Process Biochem. 2011;46(12):2336–2340. doi:
https://doi.org/10.1016/j.proc....
16.
Prendecka-Wróbel M, Pigoń-Zając D, Jaszek M, et al. Electric Cell-Substrate Impedance Sensing (ECIS) as a Convenient Tool to Assess the Potential of Low Molecular Fraction Derived from Medicinal Fungus Cerrena unicolor in Action on L929 and CT-26 Cell Lines.file:///C:/Users/UMleica02/Downloads/s11274-007-9. Molecules. 2022;27(19). doi:10.3390/molecules27196251.
17.
Guohua H, Hongyang L, Zhiming J, Danhua Z, Haifang W. Study of small-cell lung cancer cell-based sensor and its applications in chemotherapy effects rapid evaluation for anticancer drugs. Biosens Bioelectron. 2017;97:184–195. doi:10.1016/j.bios.2017.05.050.
18.
Mizerska-Dudka M, Jaszek M, Błachowicz A, et al. Fungus Cerrena unicolor as an effective source of new antiviral, immunomodulatory, and anticancer compounds. Int J Biol Macromol. 2015;79:459–468. doi:10.1016/j.ijbiomac.2015.05.015.
19.
Jaszek M, Osińska-Jaroszuk M, Janusz G, et al. New bioactive fungal molecules with high antioxidant and antimicrobial capacity isolated from Cerrena unicolor idiophasic cultures. Biomed Res Int. 2013;2013:497492. doi:10.1155/2013/497492.
20.
Leonowicz A, Grzywnowicz K. Quantitative estimation of laccase forms in some white-rot fungi using syringaldazine as a substrate. Enzyme Microb Technol. 1981;3(1):55–58. doi:
https://doi.org/10.1016/0141-0....
21.
Gariboldi MB, Marras E, Ferrario N, et al. Anti-Cancer Potential of Edible/Medicinal Mushrooms in Breast Cancer. Int J Mol Sci. 2023;24(12). doi:10.3390/ijms241210120.
22.
Song M, Cui M, Liu K. Therapeutic strategies to overcome cisplatin resistance in ovarian cancer. Eur J Med Chem. 2022;232:114205. doi:10.1016/J.EJMECH.2022.114205.
23.
Panda SK, Luyten W. Medicinal mushrooms: Clinical perspective and challenges. Drug Discov Today. 2022;27(2):636–651. doi:10.1016/j.drudis.2021.11.017.
24.
Ayeka PA. Potential of Mushroom Compounds as Immunomodulators in Cancer Immunotherapy: A Review. Evid Based Complement Alternat Med. 2018;2018:7271509. doi:10.1155/2018/7271509.
25.
Pathak MP, Pathak K, Saikia R, et al. Immunomodulatory effect of mushrooms and their bioactive compounds in cancer: A comprehensive review. Biomed Pharmacother. 2022;149:112901. doi:10.1016/j.biopha.2022.112901.
26.
Gravina AG, Pellegrino R, Auletta S, et al. Hericium erinaceus, a medicinal fungus with a centuries-old history: Evidence in gastrointestinal diseases. World J Gastroenterol. 2023;29(20):3048–3065. doi:10.3748/wjg.v29.i20.3048.
27.
Neergheen VS, Hip Kam A, Pem Y, Ramsaha S, Bahorun T. Regulation of cancer cell signaling pathways as key events for therapeutic relevance of edible and medicinal mushrooms. Semin Cancer Biol. 2022;80:145–156. doi:10.1016/j.semcancer.2020.03.004.
28.
Che X, Yan H, Sun H, et al. Grifolin induces autophagic cell death by inhibiting the Akt/mTOR/S6K pathway in human ovarian cancer cells. Oncol Rep. 2016;36(2):1041–1047. doi:10.3892/or.2016.4840.
29.
Matuszewska A, Stefaniuk D, Jaszek M, et al. Antitumor potential of new low molecular weight antioxidative preparations from the white rot fungus Cerrena unicolor against human colon cancer cells. Sci Rep. 2019;9(1):1975. doi:10.1038/s41598-018-37947-z.
30.
Pawlik A, Ciołek B, Sulej J, et al. Cerrena unicolor Laccases, Genes Expression and Regulation of Activity. Biomolecules. 2021;11(3). doi:10.3390/biom11030468.
31.
Hamilton TC, Young RC, McKoy WM, et al. Characterization of a human ovarian carcinoma cell line (NIH:OVCAR-3) with androgen and estrogen receptors. Cancer Res. 1983;43(11):5379–5389.
32.
Wegener J, Keese CR, Giaever I. Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces. Exp Cell Res. 2000;259(1):158–166. doi:10.1006/excr.2000.4919.
33.
Huang X, Nguyen D, Greve DW, Domach MM. Simulation of microelectrode impedance changes due to cell growth. IEEE Sens J. 2004;4(5):576–583. doi:10.1109/JSEN.2004.831302.
34.
Coffman FD, Cohen S. Impedance measurements in the biomedical sciences. Anal Cell Pathol. 2012;35:363–374. doi:10.3233/ACP-2012-0070.