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Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Research Article

Anticancer Activity of Sargassum fluitans Extracts in Different Cancer Cells

Author(s): José Arnold González-Garrido, Javier Alejandro Gómez-García, Oswaldo Ignacio Hernández-Abreu, Ivonne María Olivares-Corichi, Fernando Pereyra-Vergara and José Rubén García-Sánchez*

Volume 24, Issue 10, 2024

Published on: 21 February, 2024

Page: [745 - 754] Pages: 10

DOI: 10.2174/0118715206282983240215050314

Price: $65

Abstract

Background: The arrival of large quantities of Sargassum in the Mexican Caribbean Sea has generated major environmental, health and economic problems. Although Sargassum has been used in the generation of some commercial products, few studies have described its possible applications as a source of compounds with anticancer activity.

Objective: This study aimed to evaluate the antiproliferative effects of different Sargassum extracts on various cancer cell lines. Furthermore, LC/QTOF-MS was used to identify the compounds related to the antiproliferative effect.

Methods: First, determination of the seaweed was performed, and dichloromethane, chloroform and methanol extracts were obtained. The extracts were evaluated for their antiproliferative effects by MTT in breast (MDAMB- 231 and MCF-7), prostate (DU-145), lung (A549) and cervical (SiHa) cancer cell lines. Finally, LC/QTOFMS identified the compounds related to the antiproliferative effect.

Results: The authentication showed Sargassum fluitans as the predominant species. The extracts of dichloromethane and chloroform showed an antiproliferative effect. Interestingly, the fractionation of the chloroform extract showed two fractions (FC1 and FC2) with antiproliferative activity in MDA-MB-231, SiHa and A549 cancer cell lines. On the other hand, three fractions of dichloromethane extract (FD1, FD4 and FD5) also showed antiproliferative effects in the MDA-MB-231, MCF-7, SiHa and DU-145 cancer cell lines. Furthermore, LC/QTOF-MS revealed the presence of eight major compounds in FC2. Three compounds with evidence of anticancer activity were identified (D-linalool-3-glucoside, (3R,4S,6E,10Z)-3,4,7,11-tetramethyl-6,10-tridecadienal and alpha-tocotrienol).

Conclusion: These findings showed that Sargassum fluitans extracts are a possible source of therapeutic agents against cancer and could act as scaffolds for new drug discovery.

Graphical Abstract

[1]
Jonathan, M.K.; Kelly, C.; Frances, E.D.; Weijia, F.; Brian, L.G. Cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life years for 29 cancer groups from 2010 to 2019: A systematic analysis for the global burden of disease study 2019. JAMA Oncol., 2022, 8(3), 420-444.
[http://dx.doi.org/10.1001/jamaoncol.2021.6987]
[2]
D’Alterio, C.; Scala, S.; Sozzi, G.; Roz, L.; Bertolini, G. Paradoxical effects of chemotherapy on tumor relapse and metastasis promotion. Semin. Cancer Biol., 2020, 60, 351-361.
[http://dx.doi.org/10.1016/j.semcancer.2019.08.019] [PMID: 31454672]
[3]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. 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.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[4]
Dutt, R.; Garg, V.; Khatri, N.; Madan, A.K. Phytochemicals in anticancer drug development. Anticancer. Agents Med. Chem., 2019, 19(2), 172-183.
[http://dx.doi.org/10.2174/1871520618666181106115802] [PMID: 30398123]
[5]
Roleira, F.M.F.; Varela, C.L.; Costa, S.C.; Tavares-da-Silva, E.J. Phenolic derivatives from medicinal herbs and plant extracts: anticancer effects and synthetic approaches to modulate biological activity. Stu. Nat. Prod. Chem., 2018, 57, 115-156.
[http://dx.doi.org/10.1016/B978-0-444-64057-4.00004-1]
[6]
Haque, N.; Parveen, S.; Tang, T.; Wei, J.; Huang, Z. Marine natural products in clinical use. Mar. Drugs, 2022, 20(8), 528.
[http://dx.doi.org/10.3390/md20080528] [PMID: 36005531]
[7]
Khalifa, S.A.M.; Elias, N.; Farag, M.A.; Chen, L.; Saeed, A.; Hegazy, M.E.F.; Moustafa, M.S.; Abd El-Wahed, A.; Al-Mousawi, S.M.; Musharraf, S.G.; Chang, F.R.; Iwasaki, A.; Suenaga, K.; Alajlani, M.; Göransson, U.; El-Seedi, H.R. Marine natural products: A source of novel anticancer drugs. Mar. Drugs, 2019, 17(9), 491.
[http://dx.doi.org/10.3390/md17090491] [PMID: 31443597]
[8]
Rushdi, M.I.; Abdel-Rahman, I.A.M.; Saber, H.; Attia, E.Z.; Abdelraheem, W.M.; Madkour, H.A.; Hassan, H.M.; Elmaidomy, A.H.; Abdelmohsen, U.R. Pharmacological and natural products diversity of the brown algae genus Sargassum. RSC Advances, 2020, 10(42), 24951-24972.
[http://dx.doi.org/10.1039/D0RA03576A] [PMID: 35517468]
[9]
Nigam, M.; Suleria, H.A.R.; Farzaei, M.H.; Mishra, A.P. Marine anticancer drugs and their relevant targets: A treasure from the ocean. Daru, 2019, 27(1), 491-515.
[http://dx.doi.org/10.1007/s40199-019-00273-4] [PMID: 31165439]
[10]
Senthil, A.; Mamatha, B.S.; Vishwanath, P.; Bhat, K.K.; Ravishankar, G.A. Studies on development and storage stability of instant spice adjunct mix from seaweed (Eucheuma). J. Food Sci. Technol., 2011, 48(6), 712-717.
[http://dx.doi.org/10.1007/s13197-010-0165-3] [PMID: 23572809]
[11]
Bruni, R.; Barreca, D.; Protti, M.; Brighenti, V.; Righetti, L.; Anceschi, L.; Mercolini, L.; Benvenuti, S.; Gattuso, G.; Pellati, F. Botanical sources, chemistry, analysis, and biological activity of furanocoumarins of pharmaceutical interest. Molecules, 2019, 24(11), 2163.
[http://dx.doi.org/10.3390/molecules24112163] [PMID: 31181737]
[12]
Mine, I. Biological interactions during the life history of seaweed a microscopic review. Kuroshio Sci., 2008, 35-40.
[13]
Chávez, V.; Uribe-Martínez, A.; Cuevas, E.; Rodríguez-Martínez, R.E.; van Tussenbroek, B.I.; Francisco, V.; Estévez, M.; Celis, L.B.; Monroy-Velázquez, L.V.; Leal-Bautista, R.; Álvarez-Filip, L.; García-Sánchez, M.; Masia, L.; Silva, R. Massive influx of pelagic Sargassum spp. On the coasts of the Mexican Caribbean 2014–2020: Challenges and opportunities. Water, 2020, 12(10), 2908.
[http://dx.doi.org/10.3390/w12102908]
[14]
Schell, J.; Goodwin, D.; Siuda, A. Recent Sargassum inundation events in the caribbean: Shipboard observations reveal dominance of a previously rare form. Oceanography, 2015, 28(3), 8-10.
[http://dx.doi.org/10.5670/oceanog.2015.70]
[15]
Hickey, A.J.; Ganderton, D. Solid-liquid extraction. In Pharmaceutical Process Engineering; CRC Press: Taylor and Francis Group: London, UK, 2009, pp. 87-91.
[16]
Corsetto, P.A.; Montorfano, G.; Zava, S.; Colombo, I.; Ingadottir, B.; Jonsdottir, R.; Sveinsdottir, K.; Rizzo, A.M. Characterization of antioxidant potential of seaweed extracts for enrichment of convenience food. Antioxidants, 2020, 9(3), 249.
[http://dx.doi.org/10.3390/antiox9030249] [PMID: 32204441]
[17]
Saraswati, G.; Giriwono, P.E.; Iskandriati, D.; Tan, C.P.; Andarwulan, N. Sargassum seaweed as a source of anti-inflammatory substances and the potential insight of the tropical species: A review. Mar. Drugs, 2019, 17(10), 590.
[http://dx.doi.org/10.3390/md17100590]
[18]
Linch, A.L.; Hendrickson, E.R.; Katz, M.; Martin, J.R.; Nelson, G.O.; Pattison, J.N.; Vander Kolk, A.L.; Weidner, R.B. Thin-layer chromatography. Health Lab. Sci., 1973, 10(2), 141-152.
[PMID: 4701513]
[19]
Segeritz, C.P.; Vallier, L. Cell culture: Growing cells as model systems in vitro. Bas. Sci. Met. Cli. Res., 2017, 151-172.
[http://dx.doi.org/10.1016/B978-0-12-803077-6.00009-6]
[20]
Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods, 1983, 65(1-2), 55-63.
[http://dx.doi.org/10.1016/0022-1759(83)90303-4] [PMID: 6606682]
[21]
Sana, T.R.; Roark, J.C.; Li, X.; Waddell, K.; Fischer, S.M. Molecular formula and METLIN personal metabolite database matching applied to the identification of compounds generated by LC/TOF-MS. J. Biomol. Tech., 2008, 19(4), 258-266.
[PMID: 19137116]
[22]
ChemBioDraw Ultra. Available from:http://www.cambridgesoft.com/software/overview.aspx
[23]
Denningtion, R.; Roy, T.; Millam, J. Molecular docking of selective binding affinity of sulfonamide derivatives as potential antimalarial agents targeting the glycolytic enzymes: GAPDH, aldolase and TPI. In: GaussView, Version 5; Semichem Inc.: Shawnee Mission, 2009.
[24]
Frisch, M.J.; Trucks, G.W.; Schlegel, H.B. Gaussian 09, Revision A.02; Gaussian, Inc: Wallingford CT, 2016.
[25]
Morris, G.M.; Huey, R.; Lindstrom, W.; Sanner, M.F.; Belew, R.K.; Goodsell, D.S.; Olson, A.J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J. Comput. Chem., 2009, 30(16), 2785-2791.
[http://dx.doi.org/10.1002/jcc.21256] [PMID: 19399780]
[26]
DeLano, W.L. The PyMOL molecular graphics system. DeLano Scientific; San Carlos, CA,: USA, 2002. http://www.pymol.org
[27]
Amaral-Zettler, L.A.; Dragone, N.B.; Schell, J.; Slikas, B.; Murphy, L.G.; Morrall, C.E.; Zettler, E.R. Comparative mitochondrial and chloroplast genomics of a genetically distinct form of Sargassum contributing to recent “Golden Tides” in the Western Atlantic. Ecol. Evol., 2017, 7(2), 516-525.
[http://dx.doi.org/10.1002/ece3.2630] [PMID: 28116048]
[28]
Parr, A.E. Quantitative observations on the pelagic sargassum vegetation of the western north atlantic. with preliminary discussion of morphology and relationships. 1939. Available from:https://elischolar.library.yale.edu/bulletin_yale_bingham_oceanographic_collection/40
[29]
Tsuzuki, S.; Amitsuka, T.; Okahashi, T.; Kozai, Y.; Yamasaki, M.; Inoue, K.; Fushiki, T. Identification of the odor-active volatile compound (Z,Z)-4,7-tridecadienal as a potential ligand for the transmembrane receptor CD36. Biomed. Res., 2016, 37(6), 335-342.
[http://dx.doi.org/10.2220/biomedres.37.335] [PMID: 28003580]
[30]
Jiang, Y.; Guo, Y.; Hao, J.; Guenter, R.; Lathia, J.; Beck, A.W.; Hattaway, R.; Hurst, D.; Wang, Q.J.; Liu, Y.; Cao, Q.; Krontiras, H.; Chen, H.; Silverstein, R.; Ren, B. Development of an arteriolar niche and self-renewal of breast cancer stem cells by lysophosphatidic acid/protein kinase D signaling. Commun. Biol., 2021, 4(1), 780.
[http://dx.doi.org/10.1038/s42003-021-02308-6] [PMID: 34168243]
[31]
Drury, J.; Rychahou, P.G.; He, D.; Jafari, N.; Wang, C.; Lee, E.Y.; Weiss, H.L.; Evers, B.M.; Zaytseva, Y.Y. Inhibition of fatty acid synthase upregulates expression of cd36 to sustain proliferation of colorectal cancer cells. Front. Oncol., 2020, 10, 1185.
[http://dx.doi.org/10.3389/fonc.2020.01185] [PMID: 32850342]
[32]
Deng, M.; Cai, X.; Long, L.; Xie, L.; Ma, H.; Zhou, Y.; Liu, S.; Zeng, C. CD36 promotes the epithelial–mesenchymal transition and metastasis in cervical cancer by interacting with TGF-β. J. Transl. Med., 2019, 17(1), 352.
[http://dx.doi.org/10.1186/s12967-019-2098-6] [PMID: 31655604]
[33]
Yang, P.; Su, C.; Luo, X.; Zeng, H.; Zhao, L.; Wei, L.; Zhang, X.; Varghese, Z.; Moorhead, J.F.; Chen, Y.; Ruan, X.Z. Dietary oleic acid-induced CD36 promotes cervical cancer cell growth and metastasis via up-regulation Src/ERK pathway. Cancer Lett., 2018, 438, 76-85.
[http://dx.doi.org/10.1016/j.canlet.2018.09.006] [PMID: 30213558]
[34]
Watt, M.J.; Clark, A.K.; Selth, L.A.; Haynes, V.R.; Lister, N.; Rebello, R.; Porter, L.H.; Niranjan, B.; Whitby, S.T.; Lo, J.; Huang, C.; Schittenhelm, R.B.; Anderson, K.E.; Furic, L.; Wijayaratne, P.R.; Matzaris, M.; Montgomery, M.K.; Papargiris, M.; Norden, S.; Febbraio, M.; Risbridger, G.P.; Frydenberg, M.; Nomura, D.K.; Taylor, R.A. Suppressing fatty acid uptake has therapeutic effects in preclinical models of prostate cancer. Sci. Transl. Med., 2019, 11(478), eaau5758.
[http://dx.doi.org/10.1126/scitranslmed.aau5758] [PMID: 30728288]
[35]
Hsieh, F.L.; Turner, L.; Bolla, J.R.; Robinson, C.V.; Lavstsen, T.; Higgins, M.K. The structural basis for CD36 binding by the malaria parasite. Nat. Commun., 2016, 7(1), 12837.
[http://dx.doi.org/10.1038/ncomms12837] [PMID: 27667267]
[36]
Fu, C.; Xiang, M.L.; Chen, S.; Dong, G.; Liu, Z.; Chen, C.B.; Liang, J.; Cao, Y.; Zhang, M.; Liu, Q. Molecular drug simulation and experimental validation of the CD36 receptor competitively binding to long-chain fatty acids by 7-ketocholesteryl-9-carboxynonanoate. ACS Omega, 2023, 8(31), 28277-28289.
[http://dx.doi.org/10.1021/acsomega.3c02082] [PMID: 37576668]
[37]
Sugumaran, A.; Pandiyan, R.; Kandasamy, P.; Antoniraj, M.G.; Navabshan, I.; Sakthivel, B.; Dharmaraj, S.; Chinnaiyan, S.K.; Ashokkumar, V.; Ngamcharussrivichai, C. Marine biome-derived secondary metabolites, a class of promising antineoplastic agents: A systematic review on their classification, mechanism of action and future perspectives. Sci. Total Environ., 2022, 836, 155445.
[http://dx.doi.org/10.1016/j.scitotenv.2022.155445] [PMID: 35490806]
[38]
Kantarjian, H.; Short, N.J.; DiNardo, C.; Stein, E.M.; Daver, N.; Perl, A.E.; Wang, E.S.; Wei, A.; Tallman, M. Harnessing the benefits of available targeted therapies in acute myeloid leukaemia. Lancet Haematol., 2021, 8(12), e922-e933.
[http://dx.doi.org/10.1016/S2352-3026(21)00270-2] [PMID: 34687602]
[39]
Wang, J.; Wang, P.; Zeng, Z.; Lin, C.; Lin, Y.; Cao, D.; Ma, W.; Xu, W.; Xiang, Q.; Luo, L.; Wang, W.; Shi, Y.; Gao, Z.; Zhao, Y.; Liu, H.; Liu, S.L. Trabectedin in cancers: Mechanisms and clinical applications. Curr. Pharm. Des., 2022, 28(24), 1949-1965.
[http://dx.doi.org/10.2174/1381612828666220526125806] [PMID: 35619256]
[40]
Rodríguez-Martínez, R.E.; Roy, P.D.; Torrescano-Valle, N.; Cabanillas-Terán, N.; Carrillo-Domínguez, S.; Collado-Vides, L.; García-Sánchez, M.; van Tussenbroek, B.I. Element concentrations in pelagic Sargassum along the mexican caribbean coast in 2018-2019. PeerJ, 2020, 8, e8667.
[http://dx.doi.org/10.7717/peerj.8667] [PMID: 32149030]
[41]
Namvar, F.; Baharara, J.; Mahdi, A.A. Antioxidant and anticancer activities of selected persian gulf algae. Indian J. Clin. Biochem., 2014, 29(1), 13-20.
[http://dx.doi.org/10.1007/s12291-013-0313-4] [PMID: 24478544]
[42]
Namvar, F.; Mohamad, R.; Baharara, J.; Zafar-Balanejad, S.; Fargahi, F.; Rahman, H.S. Antioxidant, antiproliferative, and antiangiogenesis effects of polyphenol-rich seaweed (Sargassum muticum). BioMed. Res. Int., 2013, 2013, 1-9.
[http://dx.doi.org/10.1155/2013/604787] [PMID: 24078922]
[43]
Xu, S.Y.; Huang, X.; Cheong, K.L. Recent advances in marine algae polysaccharides: isolation, structure, and activities. Mar. Drugs, 2017, 15(12), 388.
[http://dx.doi.org/10.3390/md15120388] [PMID: 29236064]
[44]
Lin, P.; Chen, S.; Zhong, S. Nutritional and chemical composition of sargassum zhangii and the physical and chemical characterization, binding bile acid, and cholesterol-lowering activity in hepg2 cells of its fucoidans. Foods, 2022, 11(12), 1771.
[http://dx.doi.org/10.3390/foods11121771] [PMID: 35741969]
[45]
Chale-Dzul, J.; Pérez-Cabeza de Vaca, R.; Quintal-Novelo, C.; Olivera-Castillo, L.; Moo-Puc, R. Hepatoprotective effect of a fucoidan extract from Sargassum fluitans Borgesen against CCl4-induced toxicity in rats. Int. J. Biol. Macromol., 2020, 145, 500-509.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.12.183] [PMID: 31874267]
[46]
Tripathi, R.; Singh, P.; Singh, A.; Chagtoo, M.; Khan, S.; Tiwari, S.; Agarwal, G.; Meeran, S.M.; Godbole, M.M. Zoledronate and molecular iodine cause synergistic cell death in triple negative breast cancer through endoplasmic reticulum stress. Nutr. Cancer, 2016, 68(4), 679-688.
[http://dx.doi.org/10.1080/01635581.2016.1158293] [PMID: 27116040]
[47]
Chen, L.M.; Yang, P.P.; Al Haq, A.T.; Hwang, P.A.; Lai, Y.C.; Weng, Y.S.; Chen, M.A.; Hsu, H.L. Oligo-Fucoidan supplementation enhances the effect of Olaparib on preventing metastasis and recurrence of triple-negative breast cancer in mice. J. Biomed. Sci., 2022, 29(1), 70.
[http://dx.doi.org/10.1186/s12929-022-00855-6] [PMID: 36109724]
[48]
Atashrazm, F.; Lowenthal, R.; Woods, G.; Holloway, A.; Dickinson, J. Fucoidan and cancer: A multifunctional molecule with anti-tumor potential. Mar. Drugs, 2015, 13(4), 2327-2346.
[http://dx.doi.org/10.3390/md13042327] [PMID: 25874926]
[49]
van Schie, C.C.N.; Haring, M.A.; Schuurink, R.C. Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol. Biol., 2007, 64(3), 251-263.
[http://dx.doi.org/10.1007/s11103-007-9149-8] [PMID: 17440821]
[50]
Peana, A.T.; D’Aquila, P.S.; Panin, F.; Serra, G.; Pippia, P.; Moretti, M.D.L. Anti-inflammatory activity of linalool and linalyl acetate constituents of essential oils. Phytomedicine, 2002, 9(8), 721-726.
[http://dx.doi.org/10.1078/094471102321621322] [PMID: 12587692]
[51]
Chang, M.Y.; Shieh, D.E.; Chen, C.C.; Yeh, C.S.; Dong, H.P. Linalool induces cell cycle arrest and apoptosis in leukemia cells and cervical cancer cells through CDKIs. Int. J. Mol. Sci., 2015, 16(12), 28169-28179.
[http://dx.doi.org/10.3390/ijms161226089] [PMID: 26703569]
[52]
Zhao, Y.; Chen, R.; Wang, Y.; Qing, C.; Wang, W.; Yang, Y. In vitro and in vivo efficacy studies of lavender angustifolia essential oil and its active constituents on the proliferation of human prostate cancer. Integr. Cancer Ther., 2017, 16(2), 215-226.
[http://dx.doi.org/10.1177/1534735416645408] [PMID: 27151584]
[53]
Feng, W.W.; Zuppe, H.T.; Kurokawa, M. The role of cd36 in cancer progression and its value as a therapeutic target. Cells, 2023, 12(12), 1605.
[http://dx.doi.org/10.3390/cells12121605] [PMID: 37371076]
[54]
Wang, J.; Li, Y. CD36 tango in cancer: Signaling pathways and functions. Theranostics, 2019, 9(17), 4893-4908.
[http://dx.doi.org/10.7150/thno.36037] [PMID: 31410189]
[55]
Seimon, T.A.; Nadolski, M.J.; Liao, X.; Magallon, J.; Nguyen, M.; Feric, N.T.; Koschinsky, M.L.; Harkewicz, R.; Witztum, J.L.; Tsimikas, S.; Golenbock, D.; Moore, K.J.; Tabas, I. Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress. Cell Metab., 2010, 12(5), 467-482.
[http://dx.doi.org/10.1016/j.cmet.2010.09.010] [PMID: 21035758]
[56]
De Silva, L.; Chuah, L.H.; Meganathan, P.; Fu, J.Y. Tocotrienol and cancer metastasis. Biofactors, 2016, 42(2), 149-162.
[http://dx.doi.org/10.1002/biof.1259] [PMID: 26948691]
[57]
Hsieh, T.C.; Elangovan, S.; Wu, J.M. Differential suppression of proliferation in MCF-7 and MDA-MB-231 breast cancer cells exposed to alpha-, gamma- and delta-tocotrienols is accompanied by altered expression of oxidative stress modulatory enzymes. Anticancer Res., 2010, 30(10), 4169-4176. https://ar.iiarjournals.org/content/30/10/4169
[PMID: 21036737]
[58]
Lim, S.W.; Loh, H.S.; Ting, K.N.; Bradshaw, T.D.; Zeenathul, N.A. Cytotoxicity and apoptotic activities of alpha-, gamma- and delta-tocotrienol isomers on human cancer cells. BMC Complement. Altern. Med., 2014, 14(1), 469.
[http://dx.doi.org/10.1186/1472-6882-14-469] [PMID: 25480449]
[59]
Loganathan, R.; Selvaduray, K.R.; Nesaretnam, K.; Radhakrishnan, A.K. Tocotrienols promote apoptosis in human breast cancer cells by inducing poly(ADP ‐ribose) polymerase cleavage and inhibiting nuclear factor kappa‐B activity. Cell Prolif., 2013, 46(2), 203-213.
[http://dx.doi.org/10.1111/cpr.12014] [PMID: 23510475]
[60]
Ishii, K.; Hido, M.; Sakamura, M.; Virgona, N.; Yano, T. α-Tocotrienol and redox-silent analogs of vitamin E enhances bortezomib sensitivity in solid cancer cells through modulation of NFE2L1. Int. J. Mol. Sci., 2023, 24(11), 9382.
[http://dx.doi.org/10.3390/ijms24119382] [PMID: 37298331]

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