Cite this paper:
ZHOU Shengnan, LIU Ge, WU Shimei. Marine bacterial surfactin CS30-2 induced necrosis-like cell death in Huh7.5 liver cancer cells[J]. HaiyangYuHuZhao, 2020, 38(3): 826-833

Marine bacterial surfactin CS30-2 induced necrosis-like cell death in Huh7.5 liver cancer cells

ZHOU Shengnan1, LIU Ge2,3, WU Shimei1
1 College of Life Sciences, Qingdao University, Qingdao 266071, China;
2 Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
3 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
Abstract:
Marine bacterial strain Bacillus sp. CS30 exhibited high anticancer activity against Huh7.5 human liver cancer. We purified the corresponding anticancer agent by sequential acidic precipitation, methanol extraction, Sephadex LH-20 chromatography, and reversed phase high-performance liquid chromatography (RP-HPLC), then analyzed it in mass spectrometry. Based on the results of purification and mass spectrometry, we deduced that the anticancer agent was the same component as our previously purified antifungal agent surfactin CS30-2. However, to the best of our knowledge, this is the first report on the surfactin possessing both antifungal and anticancer activities. Surfactin CS30-2 was demonstrated to exhibit high anticancer activity in a dose-dependent manner against Huh7.5 liver cancer cells. Further investigation showed that surfactin CS30-2 induced the increased generation of reactive oxygen species (ROS) and severe disruption of cell membrane, thus leading to cell death. However, unlike previously reported surfactins, surfactin CS30-2 caused cancer cell death via necrosis instead of apoptosis.
Key words:    Bacillus|surfactin|anticancer activity|reactive oxygen species (ROS)   
Received: 2019-05-15   Revised: 2019-08-19
Tools
PDF (2023 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by ZHOU Shengnan
Articles by LIU Ge
Articles by WU Shimei
References:
Barzkar N, Tamadoni Jahromi S, Poorsaheli H B, Vianello F. 2019. Metabolites from marine microorganisms, micro, and macroalgae:immense scope for pharmacology. Mar.Drugs, 17(8):464.
Cadenas E, Davies K J A. 2000. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol.Med., 29(3-4):222-230.
Cao X H, Wang A H, Wang C L, Mao D Z, Lu M F, Cui Y Q, Jiao R Z. 2010. Surfactin induces apoptosis in human breast cancer MCF-7 cells through a ROS/JNK-mediated mitochondrial/caspase pathway. Chem-Biol. Interact., 183(3):357-362.
Demain A L, Sanchez S. 2009. Microbial drug discovery:80 years of progress. J. Antibiot., 62(1):5-16.
Elmore S. 2007. Apoptosis:a review of programmed cell death. Toxicol. Pathol., 35(4):495-516.
Fei F R, Hu R Y, Gong W W, Pan J, Wang M. 2019. Analysis of mortality and survival rate of liver cancer in Zhejiang Province in China:a general population-based study. Can.J. Gastroenterol. Hepatol., 2019:1074286.
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin D M, Forman D, Bray F. 2015. Cancer incidence and mortality worldwide:sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer, 136(5):E359-86.
Gudiña E J, Teixeira J A, Rodrigues L R. 2016. Biosurfactants produced by marine microorganisms with therapeutic applications. Mar. Drugs, 14(2):E38.
Hajare S N, Subramanian M, Gautam S, Sharma A. 2013.Induction of apoptosis in human cancer cells by a Bacillus lipopeptide bacillomycin D. Biochimie, 95(9):1 722-1 731.
Hermawan A, Putri H. 2018. Current report of natural product development against breast cancer stem cells. Int. J.Biochem. Cell Biol., 104:114-132.
Iwasaki A, Ohno O, Katsuyama S, Morita M, Sasazawa Y, Dan S, Simizu S, Yamori T, Suenaga K. 2015. Identification of a molecular target of kurahyne, an apoptosis-inducing lipopeptide from marine cyanobacterial assemblages.Bioorg. Med. Chem. Lett., 25(22):5 295-5 298, https://doi.org/10.1016/j.bmcl.2015.09.044.
Kuang S, Liu G, Cao R B, Zhang L L, Yu Q, Sun C M. 2017.Mansouramycin C kills cancer cells through reactive oxygen species production mediated by opening of mitochondrial permeability transition pore. Oncotarget, 8(61):104 057-104 071.
Liu G, Kuang S, Cao R B, Wang J, Peng Q C, Sun C M. 2019.Sorafenib kills liver cancer cells by disrupting SCD1-mediated synthesis of monounsaturated fatty acids via the ATP-AMPK-mTOR-SREBP1 signaling pathway. FASEB J., 33(9):10 089-10 103.
Liu G, Wang K, Kuang S, Cao R B, Bao L, Liu R, Liu H W, Sun C M. 2018. The natural compound GL22, isolated from Ganoderma mushrooms, suppresses tumor growth by altering lipid metabolism and triggering cell death.Cell Death Dis., 9(6):689, https://doi.org/10.1038/s41419-018-0731-6.
Ni C H, Yu C S, Lu H F, Yang J S, Huang H Y, Chen P Y, Wu S H, Ip S W, Chiang S Y, Lin J G, Chung J G. 2014.Chrysophanol-induced cell death (Necrosis) in human lung cancer A549 cells is mediated through increasing reactive oxygen species and decreasing the level of mitochondrial membrane potential. Environ. Toxicol., 29(7):740-749.
Obtel M, Lyoussi B, Tachfouti N, Pelissier S M, Nejjari C. 2015. Using surveillance data to understand cancer trends:an overview in Morocco. Arch. Public Health, 73:45.
Ouyang L, Shi Z, Zhao S, Wang F T, Zhou T T, Liu B, Bao J K. 2012. Programmed cell death pathways in cancer:a review of apoptosis, autophagy and programmed necrosis.Cell Prolif., 45(6):487-498.
Park S Y, Kim J H, Lee Y J, Lee S J, Kim Y. 2013. Surfactin suppresses TPA-induced breast cancer cell invasion through the inhibition of MMP-9 expression. Int. J.Oncol., 42(1):287-296.
Schinke C, Martins T, Queiroz S C N, Melo I S, Reyes F G R. 2017. Antibacterial compounds from marine bacteria, 2010-2015. J. Nat. Prod., 80(4):1 215-1 228.
Sia D, Villanueva A, Friedman S L, Llovet J M. 2017. Liver cancer cell of origin, molecular class, and effects on patient prognosis. Gastroenterology, 152(4):745-761.
Torre L A, Islami F, Siegel R L, Ward E M, Jemal A. 2017.Global cancer in women:burden and trends. Cancer Epidemiol. Biomarkers Prev., 26(4):444-457.
Valko M, Leibfritz D, Moncol J, Cronin M T D, Mazur M, Telser J. 2007. Free radicals and antioxidants in normal physiological functions and human disease. Int. J.Biochem. Cell Biol., 39(1):44-84.
Wang C L, Liu C, Niu L L, Wang L R, Hou L H, Cao X H. 2013. Surfactin-induced apoptosis through ROS-ERS-Ca2+-ERK pathways in HepG2 cells. Cell Biochem.Biophys., 67(3):1 433-1 439.
Wu S M, Liu G, Zhou S N, Sha Z X, Sun C M. 2019.Characterization of antifungal lipopeptide biosurfactants produced by marine bacterium Bacillus sp. CS30. Mar.Drugs, 17(4):199, https://doi.org/10.3390/md17040199.
Wu Y S, Ngai S C, Goh B H, Chan K G, Lee L H, Chuah L H. 2017. Anticancer activities of surfactin and potential application of nanotechnology assisted surfactin delivery.Front. Pharmacol., 8:761, https://doi.org/10.3389/fphar.2017.00761.
Xiu P Y, Liu R, Zhang D C, Sun C M. 2017. Pumilacidin-like lipopeptides derived from marine bacterium Bacillus sp.Strain 176 suppress the motility of Vibrio alginolyticus.Appl. Environ. Microbiol., 83(12):e00450-17, https://doi.org/10.1128/AEM.00450-17.
Yang H, Li X, Li X, Yu H M, Shen Z Y. 2015. Identification of lipopeptide isoforms by MALDI-TOF-MS/MS based on the simultaneous purification of iturin, fengycin, and surfactin by RP-HPLC. Anal. Bioanal. Chem., 407(9):2 529-2 542.
Zhang Y X, Yu P F, Gao Z M, Yuan J, Zhang Z. 2017. Caffeic acid n-butyl ester-triggered necrosis-like cell death in lung cancer cell line A549 is prompted by ROS mediated alterations in mitochondrial membrane potential. Eur.Rev. Med. Pharmacol. Sci., 21(7):1 665-1 671.
Zhao H B, Shao D Y, Jiang C M, Shi J L, Li Q, Huang Q S, Rajoka M S R, Yang H, Jin M L. 2017. Biological activity of lipopeptides from Bacillus. Appl. Microbiol.Biotechnol., 101(15):5 951-5 960, https://doi.org/10.1007/s00253-017-8396-0.
Zhong H Q, Xiao M Q, Zarkovic K, Zhu M J, Sa R N, Lu J H, Tao Y Z, Chen Q, Xia L, Cheng S Q, Waeg G, Zarkovic N, Yin H Y. 2017. Mitochondrial control of apoptosis through modulation of cardiolipin oxidation in hepatocellular carcinoma:a novel link between oxidative stress and cancer. Free Radical Biol. Med., 102:67-76, https://doi.org/10.1016/j.freeradbiomed.2016.10.494.
Zong W X, Ditsworth D, Bauer D E, Wang Z Q, Thompson C B. 2004. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev., 18(11):1 272-1 282.