Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

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

Research Article

Cytotoxic and Genotoxic Activities of Alkaloids from the Bulbs of Griffinia gardneriana and Habranthus itaobinus (Amaryllidaceae)

Author(s): Eduardo R. Cole, Jean P. de Andrade, João F. Allochio Filho, Elisângela F. P. Schmitt, Anderson Alves-Araújo, Jaume Bastida, Denise C. Endringer, Warley de S. Borges and Valdemar Lacerda*

Volume 19, Issue 5, 2019

Page: [707 - 717] Pages: 11

DOI: 10.2174/1871520619666190118122523

Price: $65

Abstract

Background: Amaryllidaceae plants are known to be a great source of alkaloids, which are considered an extensive group of compounds encompassing a wide range of biological activities. The remarkable cytotoxic activities observed in most of the Amaryllidaceae alkaloids derivatives have prompt the chemical and biological investigations in unexplored species from Brazil.

Objective: To evaluate the cytotoxic and genotoxic properties of alkaloids of Griffinia gardneriana and Habranthus itaobinus bulbs and study the role of caspase-3 as a molecular apoptosis mediator.

Methods: Methanolic crude extracts of Griffinia gardneriana and Habranthus itaobinus bulbs were submitted to acid-base extraction to obtain alkaloid-enriched fractions. The obtained fractions were fractionated using chromatographic techniques leading to isolation and identification of some alkaloids accomplished via HPLC and 1H-NMR, respectively. Molecular docking studies assessed the amount of free binding energy between the isolated alkaloids with the caspase-3 protein and also calculated the theoretical value of Ki. Studies have also been developed to evaluate in vitro cytotoxicity and genotoxicity in such alkaloids and apoptosis activation via the caspase pathway using both tumor and normal cell lines.

Results: Seven alkaloids were isolated and identified. Among these, 11-hydroxyvittatine and 2-α-7- dimethoxyhomolycorine were not cytotoxic, whereas tazettine, trisphaeridine, and sanguinine only showed activity against the fibroblast lineage. Lycorine and pretazettine were 10 to 30 folds more cytotoxic than the other alkaloids, including cancerous lines, and were genotoxic and capable of promoting apoptosis via the caspase-3 pathway. This result supports data obtained in docking studies wherein these two compounds exhibited the highest free energy values.

Conclusion: The cytotoxicity assay revealed that, among the seven alkaloids isolated, only lycorine and pretazettine were active against different cell lines, exhibiting concentration- and time-dependent cytotoxic actions alongside genotoxic action and the ability to induce apoptosis by caspase-3, a result consistent with those obtained in docking studies.

Keywords: Amaryllidaceae, alkaloids, Griffinia gardneriana, Habranthus itaobinus, cancer, cytotoxic activity.

« Previous
Graphical Abstract
[1]
Bastida, J.; Berkov, S.; Torras, L.; Pigni, N.B.; Andrade, J.P.; Martínez, V.; Codina, C.; Viladomat, F. Chemical and biological aspects of Amaryllidaceae alkaloids; In: Recent Advances in Pharmaceutical Sciences, Índia, Diego Muñoz-Torrero,. , 2011, pp. 65-100.
[2]
Louw, C.A.M.; Regnier, T.J.C.; Korsten, L. Medicinal bulbous plants of South Africa and their traditional relevance in the control of infectious diseases. J. Ethnopharmacol., 2002, 82, 147-154.
[3]
Dutilh, J.H.; Fernandez, E.P.; Penedo, T.S.A.; Moraes, M.M.V.; Messina, T. Livro Vermelho Flora do Brasil., Rio de Janeiro, Institutode Pesquisas Jardim Botânico do Rio de Janeiro,. 2013, 749-818.
[4]
De Andrade, J.P.; Pigni, N.B.; Torras-Claveria, L.; Guou, Y.; Berkov, S.; Reyes-Chilpac, R.; Amrani, A.E.; Zuanazzi, J.A.; Codina, C.; Viladomat, F.; Bastida, J. Alkaloids from the Hippeastrum genus: chemistry and biological activity. Rev. Latinoam. Quím., 2012, 40, 83-98.
[5]
Souza, V.C.; Lorenzi, H. Botânica Sistemática: guia ilustrado para identificação das famílias de fanerógamas nativas e exóticas no Brasil; Nova Odessa, Instituto Plantarum, 2012.
[6]
Ghavre, M.; Froese, J.; Pour, M.; Hudlicky, T. Synthesis of Amaryllidaceae Constituents and Unnatural Derivatives. Angew. Chem. Int. Ed., 2016, 55, 5642-5691.
[7]
Kilgore, M.B.; Kutchan, T.M. The amaryllidaceae alkaloids: Biosynthesis and methods for enzyme discovery. Phytochem. Rev., 2016, 15, 317-337.
[8]
Jin, Z. Amaryllidaceae and sceletium alkaloids. Nat. Prod. Rep., 2013, 30, 849-868.
[9]
Hulcová, D.; Breiterová, K.; Zemanová, L.; Siatka, T.; Šafratová, M.; Vaněčková, N.; Hošťálková, A.; Wsól, V.; Cahlíková, L. AKR1C3 inhibitory potency of naturally-occurring amaryllidaceae alkaloids of different structural types. Nat. Prod. Commun., 2017, 12, 245-246.
[10]
Unver, N. New skeletons and new concepts in amaryllidaceae alkaloids. Phytochem. Rev., 2007, 6, 125-135.
[11]
Bastida, J.; Lavilla, R.; Viladomat, F. Chemical and biological aspects of Narcissus alkaloids. Alkaloids Chem. Biol., 2006, 63, 87-179.
[12]
Nair, J.J.; Van Staden, J.; Bastida, J. Apoptosis-inducing effects of amaryllidaceae alkaloids. Curr. Med. Chem., 2016, 23, 161-185.
[13]
Mutsuga, M.; Kojima, K.; Yamashita, M.; Ohno, T.; Ogihara, Y.; Inoue, M. Inhibition of cell cycle progression trough specific phase by pancrastatin derivatives. Biol. Pharm. Bull., 2002, 25, 223-228.
[14]
Kornienko, A.; Evidente, A. Chemistry, biology, and medicinal potential of narciclasine and its congeners. Chem. Rev., 2008, 108, 1982-2014.
[15]
Mohan, K.; Deepa, R.J. Alkaloids as anticancer agents. Ann. Phytomed., 2012, 1, 46-53.
[16]
Liu, X.S.; Jiang, J.; Jiao, X.Y.; Wu, Y.E.; Lin, J.H.; Cai, Y.M. Lycorine induces apoptosis and down regulation of MCL-1 in human leukemia cells. Cancer Lett., 2009, 274, 16-24.
[17]
Wendt, J.; Radetzki, S.; Von Haefen, C.; Hemmati, P.G.; Guner, D.; Schulze-Osthoff, K.; Dorken, B.; Daniel, P.T. Induction of p21CIP/WAF-1 and G2 arrest by ionizing irradiation impedes caspase-3-mediated apoptosis in human carcinoma cells. Oncogene, 2006, 25, 972-980.
[18]
Peres, C.M.; Curi, R. Como cultivar células; Rio de Janeiro: Guanabara Koogan, 2005.
[19]
Meerow, A.W.; Snijman, D.A. Amaryllidaceae; In: Kubitzki, K. (ed.). The families and genera of vascular plants. Monocotyledons – Lilianae (except Orchidaceae).Springer-Verlag, Hamburg,. , 1998.
[20]
Dutilh, J.H.A. Revisão manuscrita da família Alliaceae, Amaryllidaceae; APNE-CNIP: Recife, Pernambuco, 2003.
[21]
Dutilh, J.H.A. Amaryllidaceae; In: Wanderley, M.G.L.; Shepherd, G.J.; Melhem, T.S.; Martins, S.E.; Kirizawa, M.; Giulietti, A.M. (Eds.). Flora fanerogâmica do estado de são paulo, são Paulo. Instituto de Botânica,. , 2005, pp. 244-256.
[22]
Oliveira, R.S.; Antoinette, J.H.A.; Sano, P.T. Habranthus (Amaryllidaceae) da cadeia do espinhaço, minas gerais e bahia, Brasil. Rodriguésia, 2010, 61, 491-503.
[23]
Dennington, R.; Keith, T.A.; Millam, J.M. GaussView, Version 5; Semichem Inc.: Shawnee Mission, KS, 2008.
[24]
Lee, C.; Yang, W.; Parr, R.G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B Condens. Matter, 1988, 37, 785-789.
[25]
Becke, A.D. Density-functional exchange-energy approximation with correct asymptotic behavior. Phys. Rev. A Gen. Phys., 1988, 38, 3098-3100.
[26]
Becke, A.D. Densityfunctional thermochemistry. III. The role of exact exchange. J. Chem. Phys., 1993, 98, 5648-5652.
[27]
Frisch, M.J.; Trucks, G.W.; Schlegel, H.B.; Scuseria, G.E.; Robb, M.A.; Cheeseman, J.R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G.A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H.P.; Izmaylov, A.F.; Bloino, J.; Zheng, G.; Sonnenberg, J.L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J.A.; Peralta, J.E.; Ogliaro, F.; Bearpark, M.; Heyd, J.J.; Brothers, E.; Kudin, K.N.; Staroverov, V.N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J.C.; Iyengar, S.S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, J.M.; Klene, M.; Knox, J.E.; Cross, J.B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R.E.; Yazyev, O.; Austin, A.J.; Cammi, R.; Pomelli, C.; Ochterski, J.W.; Martin, R.L.; Morokuma, K.; Zakrzewski, V.G.; Voth, G.A.; Salvador, P.; Dannenberg, J.J.; Dapprich, S.; Daniels, A.D.; Farkas, Ö.; Foresman, J.B.; Ortiz, J.V.; Cioslowski, J.; Fox, D.J. Gaussian 09; Gaussian, Inc.: Wallingford, CT, 2009.
[28]
Rotonda, J.; Nicholson, D.W.; Fazil, K.M.; Gallant, M.; Gareau, Y.; Labelle, M.; Peterson, E.P.; Rasper, D.M.; Ruel, R.; Vaillancourt, J.P.; Thornberry, N.A.; Becker, J.W. The three-dimensional structure of apopain/CPP32, a key mediator of apoptosis. Nat. Struct. Mol. Biol., 1996, 3, 619-625.
[29]
Trott, O.; Olson, A.J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization and multithreading. J. Comput. Chem., 2010, 31, 455-461.
[30]
Dassault Systèmes, BIOVIA BIOVIA Discovery Studio Visualizer; Release 2017, San Diego: Dassault Systèmes,. , 2016.
[31]
Mosmann, T.J. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods, 1983, 65, 55-63.
[32]
Yin, X.; Zhou, J.; Jie, C.; Xing, D.; Zhang, Y. Anticancer activity and mechanism of Scutellaria barbata extract on human lung cancer cell line A549. Life Sci., 2004, 75, 2233-2244.
[33]
Ravid, T.; Tsaba, A.; Gee, P.; Rasooly, R.; Medina, E.A.; Goldkorn, T. Ceramide accumulation precedes caspase-3 activation during apoptosis of A549 human lung adenocarcinoma cells. Am. J. Physiol. Lung Cell. Mol. Physiol., 2003, 284, 1082-1092.
[34]
Kurinna, M.S.; Tsao, C.C.; Nica, A.F.; Jiffar, T.; Ruvolo, P.P. Ceramide promotes apoptosis in lung cancer-derived A549 cells by a mechanism involving c-Jun NH2-terminal kinase. Cancer Res., 2004, 64, 7852-7856.
[35]
Fenech, M.; Chang, W.P.; Kirsch-Volders, M.; Holland, N.; Bonassi, S.; Zeiger, E. HUMN project: Detailed description of the scoring criteria for the cytokinesis-block micronucleus assay using isolated human lymphocyte cultures. Mutat. Res., 2003, 534, 65-75.
[36]
Fenech, M. Cytokinesis-block micronucleus cytome assay. Nat. Protoc., 2007, 2, 1084-1104.
[37]
Hara, R.V.; Marin-Morales, M.A. In vitro and in vivo investigation of the genotoxic potential of waters from rivers under the influence of a petroleum refinery (São Paulo State-Brazil). Chemosphere, 2017, 174, 321-330.
[38]
Della Torre, A.; Albuquerque, L.B.L.; Farrapo, N.M.; Oshima-Franco, Y.; Santos, M.G.; Tavares, R.V.S.; Rodas, A.C.D.; Dal Belo, C.A.; Cardoso, C.R.P.; Varanda, E.A.; Groppo, F.C.; Lopes, P.S. Mutagenicity induced by the hydroalcoholic extract of the medicinal plant Plathymenia reticulata Benth. J. Venom. Anim. Toxins Incl. Trop. Dis., 2011, 17, 190-198.
[39]
Pirnia, F.; Schneider, E.; Betticher, D.C.; Borner, M.M. Mitomycin C induces apoptosis and caspase-8 and -9 processing through a caspase-3 and Fas-independent pathway. Cell Death Differ., 2002, 9, 905-914.
[40]
OECD(Guideline for the Testing of Chemicals). Test Nº. 487: In vitro Mammalian Cell Micronucleus Test, OECD Guidelines for the Testing of Chemicals, Section 4,; OECD Publishing, 2010.
[41]
Fowler, P.; Whitwell, J.; Jeffrey, L.; Young, J.; Smith, K.; Kirkland, D. Etoposide; colchicine; mitomycin C and cyclophosphamide tested in the in vitro mammalian cell micronucleus test (MNvit) in Chinese Hamster Lung (CHL) cells at Covance laboratories; Harrogate UK in support of OECD draft Test Guideline 487. Mutat. Res., 2010, 702, 175-180.
[42]
Crain, W.O.; Wildman, W.C.; Roberts, J.D. Nuclear magnetic resonance spectroscopy. Carbon-13 spectra of nicotine, quinine, and some amaryllidaceae alkaloids. J. Am. Chem. Soc., 1971, 93, 990-994.
[43]
Evidente, A. Identification of 11-Hydroxyvittatine in Sternbergia lutea. J. Nat. Prod., 1986, 49, 168-169.
[44]
Ghosal, S.; Kumar, Y.; Singh, S. Glucosyloxy alkaloids from Pancratium biflorum. Phytochemistry, 1984, 23, 1167-1171.
[45]
Giordani, R.B.; De Andrade, J.P.; Verli, H.; Dutilh, J.H.; Henriques, A.T.; Berkov, S.; Bastida, J.; Zuanazzia, J.A.S. Alkaloids from Hippeastrum morelianum Lem. (Amaryllidaceae). Magn. Reson. Chem., 2011, 49, 668-672.
[46]
Likhitwitayawuid, K.; Angerhofer, C.K.; Chai, H.; Pezzuto, J.M.; Cordell, G.A.; Ruangrungsi, N. Cytotoxic and antimalarial alkaloids from the bulbs of Crinum amabile. J. Nat. Prod., 1993, 56, 1331-1338.
[47]
Mary, A.; Renko, D.Z.; Guillou, C.; Thal, C. Potent acetylcholinesterase inhibitors: design, synthesis, and structure–Activity relationships of bis-interacting ligands in the galanthamine series. Bioorg. Med. Chem., 1998, 6, 1835-1850.
[48]
Suau, R.; Gómez, A.I.; Rico, R. Ismine and related alkaloids from Lapiedra martinezii. Phytochemistry, 1990, 29, 1710-1712.
[49]
Viladomat, F.; Bastida, J.; Codina, C.; Nair, J.J.; Campbell, W.E. In: Recent Research Developments in Phytochemistry. ; Pandali,S.G. (Ed.). Trivandrum: Research Signpost Publishers, 1, pp.131- 171,. , 1997.
[50]
Zhang, F.M.; Tu, Y.Q.; Liu, J.D.; Fan, X.H.; Shi, L.; Hu, X.D.; Wang, S.H.; Zhang, Y.Q. A general approach to crinine-type Amaryllidaceae alkaloids: Total syntheses of (±)-haemanthidine, (±)-pretazettine, (±)-tazettine, and (±)-crinamine. Tetrahedron, 2006, 62, 9446-9455.
[51]
Cheng, H.; Hong, B.; Zhou, L.; Allen, J.E.; Tai, G.; Humphreys, R.; Dicker, D.T.; Liu, Y.Y.; El-Deiry, W.S. Mitomycin C potentiates TRAIL-induced apoptosis through p53-independent upregulation of death receptors: Evidence for the role of c-Jun N-terminal kinase activation. Cell Cycle, 2012, 11, 3312-3323.
[52]
Hartwell, J.L. Plants used against câncer: A survey. Lloydia, 1967, 30, 379-436.
[53]
Nair, J.J.; Bastida, J.; Viladomat, F.; Van Staden, J. Cytotoxic agents of the crinane series of amaryllidaceae alkaloids. Nat. Prod. Commun., 2012, 7, 1677-1688.
[54]
Weninger, B.; Italiano, L.; Beck, J.P.; Bastida, J.; Bergoñon, S.; Codina, C.; Lobstein, A.; Anton, R. Cytotoxic activity of amaryllidaceae alkaloids. Planta Med., 1995, 61, 77-79.
[55]
Antoun, M.D.; Mendoza, N.T.; Rios, Y.R. Cytotoxicity of Hymenocallis expansa alkaloids. J. Nat. Prod., 1993, 56, 1423-1425.
[56]
Fennell, C.W.; Van Staden, J. Crinum species in traditional and modern medicine. J. Ethnopharmacol., 2001, 78, 15-26.
[57]
Nair, J.J.; Van Staden, J. Pharmacological and toxicological insights to the South African amaryllidaceae. Food Chem. Toxicol., 2013, 62, 262-275.
[58]
Ribeiro, M.C.M.; Junior, H.L. Uso tradicional terapêutico de espécies pertencentes ao gênero vegetal Eucharis Planchon & Linden (Amaryllidaceae). Rev. Fitos, 2016, 10, 13-22.
[59]
Cabezas, F.; Argoti, J.; Martinez, S.; Codina, C.; Bastida, J.; Viladomat, F. Alcaloides y actividad biológica en Eucharis amazonica, E. grandiflora, Caliphruria subedentata y Crinum kunthianum, especies colombianas de Amaryllidaceae. Scientia Technica, 2007, 33, 237-241.
[60]
Cabezas, F.; Codina, C.; Bastidas, J.; Viladomat, F. Algunas especies colombianas de Amaryllidaceae como fuentes potenciales de inhibidores de enzimas. Universidad del Cauca; Departamento de Química, 2009, pp. 1-3.
[61]
Abou-Donia, A.H.; Amer, M.E.; Darwish, F.A.; Kassem, F.F.; Mammoda, H.M.; Abdel-Kader, M.S.; Zhou, B-N.; Kingston, D.G.I. Two new alkaloids of the crinane series from Pancratium sickenbergeri. Planta Med., 2002, 68, 379-381.
[62]
Evidente, A.; Kireev, A.S.; Jenkins, A.R.; Romero, A.E.; Steelant, W.F.A.; Slambrouck, S.V.; Kornienko, A. Biological evaluation of structurally diverse amaryllidaceae alkaloids and their synthetic derivatives: discovery of novel leads for anticancer drug design. Planta Med., 2009, 75, 501-507.
[63]
Brine, N.D.; Campbell, W.E.; Bastida, J.; Herrera, M.R.; Viladomat, F.; Codina, C.; Smith, P.J. A dinitrogenous alkaloid from Cyrthanthus obliquus. Phytochemistry, 2002, 61, 443-447.
[64]
Luo, Z.; Wang, F.; Zhang, J.; Li, X.; Zhang, M.; Hao, X.; Xue, Y.; Li, Y.; Horgen, F.D.; Yao, G.; Zhang, Y. Cytotoxic alkaloids from the whole plants of Zephyranthes candida. J. Nat. Prod., 2012, 75, 2113-2120.
[65]
Zupkó, I.; Rethy, B.; Hohmann, J.; Molnár, J.; Ocsovszki, I.; Falkay, G. Antitumor activity of alkaloids derived from amaryllidaceae species. In Vivo, 2009, 23, 41-48.
[66]
Zhan, G.; Zhou, J.; Liu, R.; Liu, T.; Guo, G.; Wang, J.; Xiang, M.; Xue, Y.; Luo, Z.; Zhang, Y.; Yao, G. Galanthamine, plicamine, and secoplicamine alkaloids from Zephyranthes candida and their anti-acetylcholinesterase and anti-inflammatory activities. J. Nat. Prod., 2016, 79, 760-766.
[67]
Berkov, S.; Codina, C.; Bastida, J. The genus Galanthus: a source of bioactive compounds. In: Rao, V. (Ed.).Phytochemicals-A ; global perspective of their role in nutrition and health. InTech. 235-254., 2012, pp.
[68]
McNulty, J.; Nair, J.J.; Bastida, J.; Pandey, S.; Griffin, C. Structure-activity studies on the lycorine pharmacophore: A potent inducer of apoptosis in human leukemia cells. Phytochemistry, 2009, 70, 913-919.
[69]
Nair, J.J.; Van Staden, J. Cytotoxicity studies of lycorine alkaloids of the Amaryllidaceae. Nat. Prod. Commun., 2014, 9, 1193-1210.
[70]
Furusawa, E.; Lum, M.K.M.; Furusawa, S. Therapeutic activity of pretazettine on Ehrlich ascites carcinoma: Adjuvant effect on standard drugs in ABC regimen. Chemotherapy, 1981, 27, 277-286.
[71]
Furusawa, E.; Furusawa, S. Therapeutic potentials of pretazettine, standard anticancer drugs, and combinations on subcutaneously implanted Lewis lung carcinoma. Chemotherapy, 1986, 32, 521-529.
[72]
Furusawa, E.; Furusawa, S. Effect of pretazettine and viva-natural, a dietary seaweed extract, on spontaneous AKR leukemia in comparison with standard drugs. Oncology, 1988, 45, 180-186.
[73]
Furusawa, E.; Furusawa, S.; Sokugawa, L. Therapeutic activity of pretazettine, standard drugs, and the combinations on intraperitoneally implanted Lewis lung carcinoma in mice. Chemotherapy, 1983, 29, 294-302.
[74]
Habli, Z.; Toumieh, G.; Fatfat, M.; Rahal, O.N.; Gali-Muhtasib, H. Emerging cytotoxic alkaloids in the battle against cancer: Overview of molecular mechanisms. Molecules, 2017, 22, 1-22.
[75]
Kumar, M.R.; Aithal, K.; Rao, B.N.; Udupa, N.; Rao, B.S. Cytotoxic, genotoxic and oxidative stress induced by 1,4-naphthoquinone in B16F1 melanoma tumor cells. Toxicol. In Vitro, 2009, 23, 242-250.
[76]
Mohammad, R.M.; Muqbil, I.; Lowe, L.; Yedjou, C.; Hsu, H.Y.; Lin, L.T.; Siegelin, M.D.; Fimognari, C.; Kumar, N.B.; Dou, Q.P.; Yang, H.; Samadi, A.K.; Russo, G.L.; Spagnuolo, C.; Ray, S.K.; Chakrabarti, M.; Morre, J.D.; Coley, H.M.; Honoki, K.; Fujii, H.; Georgakilas, A.G.; Amedei, A.; Niccolai, E.; Amin, A.; Ashraf, S.S.; Helferich, W.G.; Yang, X.; Boosani, C.S.; Guha, G.; Bhakta, D.; Ciriolo, M.R.; Aquilano, K.; Chen, S.; Mohammed, S.I.; Keith, W.N.; Bilsland, A.; Halicka, D.; Nowsheen, S.; Azmi, A.S. Broad targeting of resistance to apoptosis in cancer. Semin. Cancer Biol., 2015, 35, S78-S103.
[77]
Noble, R.L. The discovery of the vinca alkaloids--chemotherapeutic agents against cancer. Biochem. Cell Biol., 1990, 68, 1344-1351.
[78]
Simizu, S.; Takada, M.; Umezawa, K.; Imoto, M. Requirement of caspase-3(-like) protease-mediated hydrogen peroxide production for apoptosis induced by various anticancer drugs. J. Biol. Chem., 1998, 273, 26900-26907.
[79]
Yui, S.; Mikami, M.; Kitahara, M.; Yamazaki, M. The inhibitory effect of lycorine on tumor cell apoptosis induced by polymorphonuclear leukocyte-derived calprotectin. Immunopharmacology, 1998, 40, 151-162.
[80]
Liu, J.; Hu, W.X.; He, L.F.; Ye, M.; Li, Y. Effects of lycorine on HL-60 cells via arresting cell cycle and inducing apoptosis. FEBS Lett., 2004, 578, 245-250.
[81]
Nicholson, D.W.; Ali, A.; Thornberry, N.A.; Vaillancourt, J.P.; Ding, C.K.; Gallant, M.; Gareau, Y.; Griffin, P.R.; Labelle, M.; Lazebnik, Y.A.; Munday, N.A.; Raju, S.M.; Smulson, M.E.; Yamin, T-T.; Yu, V.L.; Miller, D.K. Identification and inhibition of the ICE/CED-3protease necessary for mammalian apoptosis. Nature, 1995, 376, 37-43.
[82]
Sutheesophon, K.; Nishimura, N.; Kobayashi, Y.; Furukawa, Y.; Kawano, M.; Itoh, K.; Kano, Y.; Ishii, H.; Furukawa, Y. Involvement of the Tumor Necrosis Factor (TNF)/TNF receptor system in leukemic cell apoptosis induced by histone deacetylase inhibitor depsipeptide (FK228). J. Cell. Physiol., 2005, 203, 387-397.
[83]
Wu, C.C.; Lee, S.; Malladi, S.; Chen, M.D.; Mastrandrea, N.J.; Zhang, Z.; Bratton, S.B. The Apaf-1 apoptosome induces formation of caspase-9 homo- and heterodimers with distinct activities. Nat. Commun., 2016, 7, 1-14.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy