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Letters in Drug Design & Discovery

Author(s): Uzma Faridi*

DOI: 10.2174/1570180819666220523092459

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Plant Secondary Metabolites as Apoptosis-inducing Agents

Page: [375 - 385] Pages: 11

  • * (Excluding Mailing and Handling)

Abstract

Apoptosis or programmed cell death is a carefully synchronized collapse of cells due to protein degradation and fragmentation of DNA. It is an essential part of the life cycle of every multicellular organism, including worms to humans. Apoptosis plays a major role in cancer development as well. Various studies confirm the potential of many drugs to change the regulation and ratio of pro-apoptotic and antiapoptotic factors. Plants are the best-known source of drugs for various diseases, including cancer. Plant secondary metabolites (alkaloids, terpenes and phenolics) are the major constituents used as drugs. Several studies confirm that these secondary metabolites can induce apoptosis by triggering pro-apoptotic and antiapoptotic factors. This article has studied some of the important secondary metabolites and their mode of action as apoptotic triggering agents.

Keywords: Plants secondary metabolites, alkaloids, terpenes, phenolics, apoptosis, anticancer

Graphical Abstract

[1]
Heilmann, J. New medical applications of plant secondary metabolites. Annu. plant rev., 2018, 39, 348-380.
[2]
Newman, D.J.; Cragg, G.M. Natural products as sources of new drugs over the last 25 years. J. Nat. Prod., 2007, 70(3), 461-477.
[http://dx.doi.org/10.1021/np068054v] [PMID: 17309302]
[3]
Potterat, O.; Hamburger, M. Drug discovery and development with plant-derived compounds. Natural Compounds as Drugs, 2008, I, 4 5-118.
[4]
Upadhyay, H.C. Medicinal chemistry of alternative therapeutics: Novelty and hopes with genus ammannia. Curr. Top. Med. Chem., 2019, 19(10), 784-794.
[http://dx.doi.org/10.2174/1568026619666190412101047] [PMID: 30977452]
[5]
Pereira, D.M.; Valentao, P.; Correia-da-Silva, G.; Teixeira, N.; Andrade, P.B. Plant secondary metabolites in cancer chemotherapy: Where are we? Curr. Pharm. Biotechnol., 2012, 13(5), 632-650.
[http://dx.doi.org/10.2174/138920112799857530] [PMID: 22122478]
[6]
Lee, M.R. The history of Ephedra (ma-huang). R Coll Physicians Edinb, 2011, 41(1), 78-84.
[http://dx.doi.org/10.4997/JRCPE.2011.116] [PMID: 21365072]
[7]
Mawalagedera, S.M.; Callahan, D.L.; Gaskett, A.C.; Rønsted, N.; Symonds, M.R. Combining evolutionary inference and metabolomics to identify plants with medicinal potential. Front. Ecol. Evol., 2019, 7, 267.
[http://dx.doi.org/10.3389/fevo.2019.00267]
[8]
Kyriazis, M. Neuroprotective, anti-apoptotic effects of apomorphine. J. Anti Aging Med., 2003, 6(1), 21-28.
[http://dx.doi.org/10.1089/109454503765361551] [PMID: 12941180]
[9]
Lee, J.Y.; Ham, J.; Lim, W.; Song, G. Apomorphine induces mitochondrial-dysfunction-dependent apoptosis in choriocarcinoma. Reproduction, 2020, 160(3), 367-377.
[http://dx.doi.org/10.1530/REP-20-0230] [PMID: 32520723]
[10]
Hara, H.; Ohta, M.; Ohta, K.; Kuno, S.; Adachi, T. Apomorphine attenuates 6-hydroxydopamine-induced apoptotic cell death in SH-SY5Y cells. Redox Rep., 2003, 8(4), 193-197.
[http://dx.doi.org/10.1179/135100003225002682] [PMID: 14599342]
[11]
Pardini, C.; Vaglini, F.; Galimberti, S.; Corsini, G.U. Dose-dependent induction of apoptosis by R-apomorphine in CHO-K1 cell line in culture. Neuropharmacology, 2003, 45(2), 182-189.
[http://dx.doi.org/10.1016/S0028-3908(03)00152-7] [PMID: 12842124]
[12]
Chen, J.; Zhao, H.; Wang, X.; Lee, F.S.C.; Yang, H.; Zheng, L. Analysis of major alkaloids in Rhizoma coptidis by capillary electrophoresis-electrospray-time of flight mass spectrometry with different background electrolytes. Electrophoresis, 2008, 29(10), 2135-2147.
[http://dx.doi.org/10.1002/elps.200700797] [PMID: 18425753]
[13]
Yu, H.H.; Kim, K.J.; Cha, J.D.; Kim, H.K.; Lee, Y.E.; Choi, N.Y.; You, Y.O. Antimicrobial activity of berberine alone and in combination with ampicillin or oxacillin against methicillin-resistant Staphylococcus aureus. J. Med. Food, 2005, 8(4), 454-461.
[http://dx.doi.org/10.1089/jmf.2005.8.454] [PMID: 16379555]
[14]
Lau, C.W.; Yao, X.Q.; Chen, Z.Y.; Ko, W.H.; Huang, Y. Cardiovascular actions of berberine. Cardiovasc. Drug Rev., 2001, 19(3), 234-244.
[http://dx.doi.org/10.1111/j.1527-3466.2001.tb00068.x] [PMID: 11607041]
[15]
Kulkarni, S.K.; Dhir, A. Berberine: A plant alkaloid with therapeutic potential for central nervous system disorders. Phytother. Res., 2010, 24(3), 317-324.
[http://dx.doi.org/10.1002/ptr.2968] [PMID: 19998323]
[16]
Sun, Y.; Xun, K.; Wang, Y.; Chen, X. A systematic review of the anticancer properties of berberine, a natural product from Chinese herbs. Anticancer Drugs, 2009, 20(9), 757-769.
[http://dx.doi.org/10.1097/CAD.0b013e328330d95b] [PMID: 19704371]
[17]
Diogo, C.V.; Machado, N.G.; Barbosa, I.A.; Serafim, T.L.; Burgeiro, A.; Oliveira, P.J. Berberine as a promising safe anti-cancer agent - is there a role for mitochondria? Curr. Drug Targets, 2011, 12(6), 850-859.
[http://dx.doi.org/10.2174/138945011795528930] [PMID: 21269266]
[18]
Tan, W.; Lu, J.; Huang, M.; Li, Y.; Chen, M.; Wu, G.; Wang, Y. Anticancer natural products isolated from chinese medicinal herbs. Chin. Med., 2011, 6(1), 1-15.
[http://dx.doi.org/10.1186/1749-8546-6-27] [PMID: 21226952]
[19]
Eom, K.S.; Kim, H.J.; So, H.S.; Park, R.; Kim, T.Y. Berberine-induced apoptosis in human glioblastoma T98G cells is mediated by endoplasmic reticulum stress accompanying reactive oxygen species and mitochondrial dysfunction. Biol. Pharm. Bull., 2010, 33(10), 1644-1649.
[http://dx.doi.org/10.1248/bpb.33.1644] [PMID: 20930370]
[20]
Chang, K.S.S.; Gao, C.; Wang, L.C. Berberine-induced morphologic differentiation and down-regulation of c-Ki-ras2 protooncogene expression in human teratocarcinoma cells. Cancer Lett., 1990, 55(2), 103-108.
[http://dx.doi.org/10.1016/0304-3835(90)90018-S] [PMID: 2265407]
[21]
Lu, J.J.; Bao, J.L.; Chen, X.P.; Huang, M.; Wang, Y.T. Alkaloids isolated from natural herbs as the anticancer agents. Evid. Based Complement. Alternat. Med., 2012, 2012, 485042.
[http://dx.doi.org/10.1155/2012/485042] [PMID: 22988474]
[22]
O’Brien, P.; Carrasco-Pozo, C.; Speisky, H. Boldine and its antioxidant or health-promoting properties. Chem. Biol. Interact., 2006, 159(1), 1-17.
[http://dx.doi.org/10.1016/j.cbi.2005.09.002] [PMID: 16221469]
[23]
Hengartner, M.O. The biochemistry of apoptosis. Nature, 2000, 407(6805), 770-776.
[http://dx.doi.org/10.1038/35037710] [PMID: 11048727]
[24]
Mochizuki, T.; Asai, A.; Saito, N.; Tanaka, S.; Katagiri, H.; Asano, T.; Nakane, M.; Tamura, A.; Kuchino, Y.; Kitanaka, C.; Kirino, T. Akt protein kinase inhibits non-apoptotic programmed cell death induced by ceramide. J. Biol. Chem., 2002, 277(4), 2790-2797.
[http://dx.doi.org/10.1074/jbc.M106361200] [PMID: 11706021]
[25]
Gerhardt, D.; Bertola, G.; Dietrich, F.; Figueiro, F.; Zanotto-Filho, A.; Fonseca, J.C.M.; Salbego, C.G. Boldine induces cell cycle arrest and apoptosis in T24 human bladder cancer cell line via regulation of ERK, AKT, and GSK-3β. In Urologic Oncology: Seminars and Original Investigations, 2014, 32(1), 36-e1.
[26]
Noureini, S.K.; Wink, M. Dose-dependent cytotoxic effects of boldine in HepG-2 cells-telomerase inhibition and apoptosis induction. Molecules, 2015, 20(3), 3730-3743.
[http://dx.doi.org/10.3390/molecules20033730] [PMID: 25719742]
[27]
Hwang, J.M.; Kuo, H.C.; Tseng, T.H.; Liu, J.Y.; Chu, C.Y. Berberine induces apoptosis through a mitochondria/caspases pathway in human hepatoma cells. Arch. Toxicol., 2006, 80(2), 62-73.
[http://dx.doi.org/10.1007/s00204-005-0014-8] [PMID: 16189662]
[28]
Bonfoco, E.; Ceccatelli, S.; Manzo, L.; Nicotera, P. Colchicine induces apoptosis in cerebellar granule cells. Exp. Cell Res., 1995, 218(1), 189-200.
[http://dx.doi.org/10.1006/excr.1995.1147] [PMID: 7537689]
[29]
Nakagawa-Yagi, Y.; Choi, D.K.; Ogane, N.; Shimada, S.; Seya, M.; Momoi, T.; Ito, T.; Sakaki, Y. Discovery of a novel compound: Insight into mechanisms for acrylamide-induced axonopathy and colchicine-induced apoptotic neuronal cell death. Brain Res., 2001, 909(1-2), 8-19.
[http://dx.doi.org/10.1016/S0006-8993(01)02608-7] [PMID: 11478917]
[30]
Zhang, T.; Chen, W.; Jiang, X.; Liu, L.; Wei, K.; Du, H.; Wang, H.; Li, J. Anticancer effects and underlying mechanism of Colchicine on human gastric cancer cell lines in vitro and in vivo. Biosci. Rep., 2019, 39(1), BSR20181802.
[http://dx.doi.org/10.1042/BSR20181802] [PMID: 30429232]
[31]
Huang, Z.; Xu, Y.; Peng, W. Colchicine induces apoptosis in HT 29 human colon cancer cells via the AKT and c-Jun N-terminal kinase signaling pathways. Mol. Med. Rep., 2015, 12(4), 5939-5944.
[http://dx.doi.org/10.3892/mmr.2015.4222] [PMID: 26299305]
[32]
Mitscher, L.A.; Park, Y.H.; Clark, D.; Clark, G.W., III; Hammesfahr, P.D.; Wu, W.N.; Beal, J.L. Antimicrobial agents from higher plants. An investigation of Hunnemannia fumariaefolia pseudoalcoholates of sanguinarine and chelerythrine. Lloydia, 1978, 41(2), 145-150.
[PMID: 651561]
[33]
Yu, H.; Pardoll, D.; Jove, R. STATs in cancer inflammation and immunity: A leading role for STAT3. Nat. Rev. Cancer, 2009, 9(11), 798-809.
[http://dx.doi.org/10.1038/nrc2734] [PMID: 19851315]
[34]
Zhang, J.; Ahn, K.S.; Kim, C.; Shanmugam, M.K.; Siveen, K.S.; Arfuso, F.; Samym, R.P.; Deivasigamanim, A.; Lim, L.H.; Wang, L.; Goh, B.C.; Kumar, A.P.; Hui, K.M.; Sethi, G. Nimbolide-induced oxidative stress abrogates STAT3 signaling cascade and inhibits tumor growth in transgenic adenocarcinoma of mouse prostate model. Antioxid. Redox Signal., 2016, 24(11), 575-589.
[http://dx.doi.org/10.1089/ars.2015.6418] [PMID: 26649526]
[35]
Chen, X.; Dai, X.; Zou, P.; Chen, W.; Rajamanickam, V.; Feng, C.; Zhuge, W.; Qiu, C.; Ye, Q.; Zhang, X.; Liang, G. Curcuminoid EF24 enhances the anti-tumour activity of Akt inhibitor MK-2206 through ROS-mediated endoplasmic reticulum stress and mitochondrial dysfunction in gastric cancer. Br. J. Pharmacol., 2017, 174(10), 1131-1146.
[http://dx.doi.org/10.1111/bph.13765] [PMID: 28255993]
[36]
Banerjee, K.; Resat, H. Constitutive activation of STAT3 in breast cancer cells: A review. Int. J. Cancer, 2016, 138(11), 2570-2578.
[http://dx.doi.org/10.1002/ijc.29923] [PMID: 26559373]
[37]
Haura, E.B.; Zheng, Z.; Song, L.; Cantor, A.; Bepler, G. Activated epidermal growth factor receptor-Stat-3 signaling promotes tumor survival in vivo in non-small cell lung cancer. Clin. Cancer Res., 2005, 11(23), 8288-8294.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-0827] [PMID: 16322287]
[38]
Yang, R.; Tavares, M.T.; Teixeira, S.F.; Azevedo, R.A.; C Pietro, D. ; Fernandes, T.B.; Ferreira, A.K.; Trossini, G.H.G.; Barbuto, J.A.M.; Parise-Filho, R. Toward chelerythrine optimization: Analogues designed by molecular simplification exhibit selective growth inhibition in non-small-cell lung cancer cells. Bioorg. Med. Chem., 2016, 24(19), 4600-4610.
[http://dx.doi.org/10.1016/j.bmc.2016.07.065] [PMID: 27561984]
[39]
Malikova, J.; Zdarilova, A.; Hlobilkova, A. Effects of sanguinarine and chelerythrine on the cell cycle and apoptosis. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub., 2006, 150(1), 5-12.
[http://dx.doi.org/10.5507/bp.2006.001] [PMID: 16936897]
[40]
Tang, J.Y.; Ou-Yang, F.; Hou, M.F.; Huang, H.W.; Wang, H.R.; Li, K.T.; Fayyaz, S.; Shu, C.W.; Chang, H.W.; Chang, H.W. Oxidative stress-modulating drugs have preferential anticancer effects - involving the regulation of apoptosis, DNA damage, endoplasmic reticulum stress, autophagy, metabolism, and migration. Semin. Cancer Biol., 2019, 58, 109-117.
[http://dx.doi.org/10.1016/j.semcancer.2018.08.010] [PMID: 30149066]
[41]
He, H.; Zhuo, R.; Dai, J.; Wang, X.; Huang, X.; Wang, H.; Xu, D. Chelerythrine induces apoptosis via ROS-mediated endoplasmic reticulum stress and STAT3 pathways in human renal cell carcinoma. J. Cell. Mol. Med., 2020, 24(1), 50-60.
[http://dx.doi.org/10.1111/jcmm.14295] [PMID: 31568643]
[42]
Akinboye, S Biological activities of emetine. Open Nat. Prod. J, 2011, 4(1)
[43]
Wiegrebe, W.; Kramer, W.J.; Shamma, M. The emetine alkaloids. J. Nat. Prod., 1984, 47(3), 397-408.
[http://dx.doi.org/10.1021/np50033a001]
[44]
Hadden, J.W.; Pascarelli, E.F. Diagnosis and treatment of human fascioliasis. JAMA, 1967, 202(2), 149-151.
[http://dx.doi.org/10.1001/jama.1967.03130150117030] [PMID: 6072213]
[45]
Bicknell, G.R.; Snowden, R.T.; Cohen, G.M. Formation of high molecular mass DNA fragments is a marker of apoptosis in the human leukaemic cell line, U937. J. Cell Sci., 1994, 107(Pt 9), 2483-2489.
[http://dx.doi.org/10.1242/jcs.107.9.2483] [PMID: 7844165]
[46]
Watanabe, N.; Iwamoto, T.; Dickinson, D.A.; Iles, K.E.; Forman, H.J. Activation of the mitochondrial caspase cascade in the absence of protein synthesis does not require c-Jun N-terminal kinase. Arch. Biochem. Biophys., 2002, 405(2), 231-240.
[http://dx.doi.org/10.1016/S0003-9861(02)00399-5] [PMID: 12220537]
[47]
Möller, M.; Weiss, J.; Wink, M. Reduction of cytotoxicity of the alkaloid emetine through P-glycoprotein (MDR1/ABCB1) in human Caco-2 cells and leukemia cell lines. Planta Med., 2006, 72(12), 1121-1126.
[http://dx.doi.org/10.1055/s-2006-941546] [PMID: 16783693]
[48]
Meijerman, I.; Blom, W.M.; de Bont, H.J.G.M.; Mulder, G.J.; Nagelkerke, J.F. Induction of apoptosis and changes in nuclear G-actin are mediated by different pathways: The effect of inhibitors of protein and RNA synthesis in isolated rat hepatocytes. Toxicol. Appl. Pharmacol., 1999, 156(1), 46-55.
[http://dx.doi.org/10.1006/taap.1998.8616] [PMID: 10101098]
[49]
Grollman, A.P. Structural basis for inhibition of protein synthesis by emetine and cycloheximide based on an analogy between ipecac alkaloids and glutarimide antibiotics. Proc. Natl. Acad. Sci. USA, 1966, 56(6), 1867-1874.
[http://dx.doi.org/10.1073/pnas.56.6.1867] [PMID: 16591432]
[50]
Grollman, A.P. Inhibitors of protein biosynthesis. V. Effects of emetine on protein and nucleic acid biosynthesis in HeLa cells. J. Biol. Chem., 1968, 243(15), 4089-4094.
[http://dx.doi.org/10.1016/S0021-9258(18)93283-7] [PMID: 4299101]
[51]
Möller, M.; Herzer, K.; Wenger, T.; Herr, I.; Wink, M. The alkaloid emetine as a promising agent for the induction and enhancement of drug-induced apoptosis in leukemia cells. Oncol. Rep., 2007, 18(3), 737-744.
[http://dx.doi.org/10.3892/or.18.3.737] [PMID: 17671728]
[52]
Möller, M.; Wink, M. Characteristics of apoptosis induction by the alkaloid emetine in human tumour cell lines. Planta Med., 2007, 73(13), 1389-1396.
[http://dx.doi.org/10.1055/s-2007-990229] [PMID: 17912675]
[53]
Crowell, P.L. Monoterpenes in breast cancer chemoprevention. Breast Cancer Res. Treat., 1997, 46(2-3), 191-197.
[http://dx.doi.org/10.1023/A:1005939806591] [PMID: 9478274]
[54]
Crowell, P.L. Prevention and therapy of cancer by dietary monoterpenes. J. J. Nutr., 1999, 129(3), 775-778.
[http://dx.doi.org/10.1093/jn/129.3.775S]
[55]
Dudareva, N.; Andersson, S.; Orlova, I.; Gatto, N.; Reichelt, M.; Rhodes, D.; Boland, W.; Gershenzon, J. The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc. Natl. Acad. Sci. USA, 2005, 102(3), 933-938.
[http://dx.doi.org/10.1073/pnas.0407360102] [PMID: 15630092]
[56]
Theis, N.; Lerdau, M. The evolution of function in plant secondary metabolites. Int. J. Plant Sci., 2003, 164(S3), 93-103.
[http://dx.doi.org/10.1086/374190]
[57]
Paduch, R. Kandefer-Szerszeń M.; Trytek, M.; Fiedurek, J. Terpenes: Substances useful in human healthcare. Arch. Immunol. Ther. Exp. (Warsz.), 2007, 55(5), 315-327.
[http://dx.doi.org/10.1007/s00005-007-0039-1] [PMID: 18219762]
[58]
Dabbah, R.; Edwards, V.M.; Moats, W.A. Antimicrobial action of some citrus fruit oils on selected food-borne bacteria. Appl. Microbiol., 1970, 19(1), 27-31.
[http://dx.doi.org/10.1128/am.19.1.27-31.1970] [PMID: 4905947]
[59]
Sayyah, M.; Nadjafnia, L.; Kamalinejad, M. Anticonvulsant activity and chemical composition of Artemisia dracunculus L. essential oil. J. Ethnopharmacol., 2004, 94(2-3), 283-287.
[http://dx.doi.org/10.1016/j.jep.2004.05.021] [PMID: 15325732]
[60]
Wang, Y.; Yi, L.; Liang, Y.; Li, H.; Yuan, D.; Gao, H.; Zeng, M. Comparative analysis of essential oil components in Pericarpium Citri Reticulatae Viride and Pericarpium Citri Reticulatae by GC-MS combined with chemometric resolution method. J. Pharm. Biomed. Anal., 2008, 46(1), 66-74.
[http://dx.doi.org/10.1016/j.jpba.2007.08.030] [PMID: 17942260]
[61]
Erasto, P.; Viljoen, A. M. Limonene-a review: Biosynthetic, ecological and pharmacological relevance. Nat. Prod. Commun., 2008, 3(7), 1934578X0800300728.
[http://dx.doi.org/10.1177/1934578X0800300728]
[62]
Kummer, R.; Fachini-Queiroz, F.C.; Estevão-Silva, C.F.; Grespan, R.; Silva, E.L.; Bersani-Amado, C.A.; Cuman, R.K.N. Evaluation of anti-inflammatory activity of Citrus latifolia Tanaka essential oil and limonene in experimental mouse models; Evid. Based Complementary Altern, 2013.
[63]
Piccinelli, A.C.; Morato, P.N.; Dos Santos Barbosa, M.; Croda, J.; Sampson, J.; Kong, X.; Konkiewitz, E.C.; Ziff, E.B.; Amaya-Farfan, J.; Kassuya, C.A. Limonene reduces hyperalgesia induced by gp120 and cytokines by modulation of IL-1 β and protein expression in spinal cord of mice. Life Sci., 2017, 174, 28-34.
[http://dx.doi.org/10.1016/j.lfs.2016.11.017] [PMID: 27888114]
[64]
Kamalakkannan, N.; Prince, P. Antidiabetic and anti-oxidant activity of Aegle marmelos extract in streptozotocin-induced diabetic rats. Pharm. Biol., 2004, 42(2), 125-130.
[http://dx.doi.org/10.1080/13880200490510937]
[65]
Vieira, A.J.; Beserra, F.P.; Souza, M.C.; Totti, B.M.; Rozza, A.L. Limonene: Aroma of innovation in health and disease. Chem. Biol. Interact., 2018, 283, 97-106.
[http://dx.doi.org/10.1016/j.cbi.2018.02.007] [PMID: 29427589]
[66]
Bai, J.; Zheng, Y.; Wang, G.; Liu, P. Protective effect of Dlimonene against oxidative stress-induced cell damage in human lens epithelial cells via the p38 pathway. Oxid. Med. Cell. Longev., 1/2016, 5962832.
[http://dx.doi.org/10.1155/2016/5962832] [PMID: 26682012]
[67]
Sabu, M.C.; Kuttan, R. Antidiabetic activity of Aegle marmelos and its relationship with its antioxidant properties. Indian J. Physiol. Pharmacol., 2004, 48(1), 81-88.
[PMID: 15270373]
[68]
Shojaei, S.; Kiumarsi, A.; Moghadam, A.R.; Alizadeh, J.; Marzban, H.; Ghavami, S. Perillyl alcohol (monoterpene alcohol), limonene. Enzymes, 2014, 36, 7-32.
[http://dx.doi.org/10.1016/B978-0-12-802215-3.00002-1] [PMID: 27102697]
[69]
Kelloff, G.J.; Boone, C.W.; Crowell, J.A.; Steele, V.E.; Lubet, R.A.; Doody, L.A.; Malone, W.F.; Hawk, E.T.; Sigman, C.C. New agents for cancer chemoprevention. J. Cell. Biochem. Suppl., 1996, 26, 1-28.
[http://dx.doi.org/10.1002/(SICI)1097-4644(1996)25+<1::AIDJCB1>3.0.CO;2-4] [PMID: 9154166]
[70]
Buckle, J. Basic plant taxonomy, chemistry, extraction, biosynthesis, and analysis.Clinical aromatherapy. Essential Oils in Practice, Ed.3; Buckle, Jane, Ed.; Elsevier Science, 2003, pp. 38-75.
[71]
Garcia, D.G.; Amorim, L.M.; de Castro Faria, M.V.; Freire, A.S.; Santelli, R.E.; Da Fonseca, C.O.; Quirico-Santos, T.; Burth, P. The anticancer drug perillyl alcohol is a Na/K-ATPase inhibitor. Mol. Cell. Biochem., 2010, 345(1-2), 29-34.
[http://dx.doi.org/10.1007/s11010-010-0556-9] [PMID: 20689980]
[72]
Belanger, J.T. Perillyl alcohol: Applications in oncology. Altern. Med. Rev., 1998, 3(6), 448-457.
[PMID: 9855569]
[73]
Stayrook, K.R.; McKinzie, J.H.; Barbhaiya, L.H.; Crowell, P.L. Effects of the antitumor agent perillyl alcohol on H-Ras vs. K-Ras farnesylation and signal transduction in pancreatic cells. Anticancer Res., 1998, 18(2A), 823-828.
[PMID: 9615726]
[74]
Singh, P.; Sharma, S. Triterpenoid constituents of the seeds of diospyros melanoxylon, tecomellaundulata and terminalia bellirica. J. Indian Chem. Soc., 1997, 74(6), 504-505.
[75]
Schühly, W.; Heilmann, J.; Calis, I.; Sticher, O. New triterpenoids with antibacterial activity from Zizyphus joazeiro. Planta Med., 1999, 65(8), 740-743.
[http://dx.doi.org/10.1055/s-1999-14054] [PMID: 10630117]
[76]
Moghaddam, M.G.; Ahmad, F.B.H.; Samzadeh-Kermani, A. Biological activity of betulinic acid: A review. J. Pharm. Pharmacol., 2012, 3(2), 119-123.
[http://dx.doi.org/10.4236/pp.2012.32018]
[77]
Pisha, E.; Chai, H.; Lee, I.S.; Chagwedera, T.E.; Farnsworth, N.R.; Cordell, G.A.; Beecher, C.W.; Fong, H.H.; Kinghorn, A.D.; Brown, D.M.; Wani, M.C.; Wall, M.E.; Hieken, T.J.; Das Gupta, T.K.; Pezzuto, J.M. Discovery of betulinic acid as a selective inhibitor of human melanoma that functions by induction of apoptosis. Nat. Med., 1995, 1(10), 1046-1051.
[http://dx.doi.org/10.1038/nm1095-1046] [PMID: 7489361]
[78]
Fulda, S.; Scaffidi, C.; Susin, S.A.; Krammer, P.H.; Kroemer, G.; Peters, M.E.; Debatin, K.M. Activation of mitochondrial apoptogenic factors by betulinic acid. J. Biol. Chem., 1998, 273, 33942-33948.
[http://dx.doi.org/10.1074/jbc.273.51.33942] [PMID: 9852046]
[79]
Satyaveanthan, M.V.; Suhaimi, S.A.; Ng, C.L.; Muhd-Noor, N.D.; Awang, A.; Lam, K.W.; Hassan, M. Purification, biochemical characterisation and bioinformatic analysis of recombinant farnesol dehydrogenase from Theobroma cacao. Plant Physiol. Biochem., 2021, 161, 143-155.
[http://dx.doi.org/10.1016/j.plaphy.2021.01.050] [PMID: 33588320]
[80]
Kossakowska-Zwierucho, M.; Szewczyk, G.; Sarna, T.; Nakonieczna, J. Farnesol potentiates photodynamic inactivation of Staphylococcus aureus with the use of red light-activated porphyrin TMPyP. J. Photochem. Photobiol. B, 2020, 206, 111863.
[http://dx.doi.org/10.1016/j.jphotobiol.2020.111863] [PMID: 32224392]
[81]
Machida, K.; Tanaka, T.; Fujita, K.; Taniguchi, M. Farnesol-induced generation of reactive oxygen species via indirect inhibition of the mitochondrial electron transport chain in the yeast Saccharomyces cerevisiae. J. Bacteriol., 1998, 180(17), 4460-4465.
[http://dx.doi.org/10.1128/JB.180.17.4460-4465.1998] [PMID: 9721283]
[82]
Joo, J.H.; Jetten, A.M. Molecular mechanisms involved in farnesol-induced apoptosis. Cancer Lett., 2010, 287(2), 123-135.
[http://dx.doi.org/10.1016/j.canlet.2009.05.015] [PMID: 19520495]
[83]
Faridi, U. Fahad, Al-Mutairi In silico anticancer targets of L-menthol. Int. J. Biosci., 2019, 15(4), 248-253.
[84]
Faridi, U.; Sisodia, B.S.; Shukla, A.K.; Shukla, R.K.; Darokar, M.P.; Dwivedi, U.N.; Shasany, A.K. Proteomics indicates modulation of tubulin polymerization by L-menthol inhibiting human epithelial colorectal adenocarcinoma cell proliferation. Proteomics, 2011, 11(10), 2115-2119.
[http://dx.doi.org/10.1002/pmic.201000691] [PMID: 21472860]
[85]
Lin, J.P.; Lu, H.F.; Lee, J.H.; Lin, J.G.; Hsia, T.C.; Wu, L.T.; Chung, J.G. (-)-Menthol inhibits DNA topoisomerases I, II α and β and promotes NF-kappaB expression in human gastric cancer SNU-5 cells. Anticancer Res., 2005, 25(3B), 2069-2074.
[PMID: 16158947]
[86]
Ramanoelina, A.R.; Terrom, G.P.; Bianchini, J.P.; Coulanges, P. Antibacterial action of essential oils extracted from Madagascar plants. Arch. Inst. Pasteur Madagascar, 1987, 53(1), 217-226.
[PMID: 3451708]
[87]
Robin, V.; Boustie, J.; Amoros, M.; Girre, L. In vitro Antiviral activity of seven Psiadia species, Asteraceae: Isolation of two antipoliovirus flavonoids from Psiadia dentata. Pharm. Pharmacol. Commun., 1998, 4, 61-64.
[88]
Koch, A.; Tamez, P.; Pezzuto, J.; Soejarto, D. Evaluation of plants used for antimalarial treatment by the Maasai of Kenya. J. Ethnopharmacol., 2005, 101(1-3), 95-99.
[http://dx.doi.org/10.1016/j.jep.2005.03.011] [PMID: 15878245]
[89]
Githinji, E.K.; Irungu, L.W.; Tonui, W.K.; Rukunga, G.M.; Mutai, C.; Muthaura, C.N.; Lugalia, R.; Gikandi, G.; Wainaina, C.W.; Ingonga, J.M.; Wanjoya, A. In vitro effects of Warburgia ugandensis, Psiadia punctulata and Chasmanthera dependens on Leishmania major promastigotes. Afr. J. Tradit. Complement. Altern. Med., 2010, 7(3), 264-275.
[http://dx.doi.org/10.4314/ajtcam.v7i3.54791] [PMID: 21461155]
[90]
Mahadeo, K.; Grondin, I.; Kodja, H.; Soulange Govinden, J.; Jhaumeer Laulloo, S.; Frederich, M.; Gauvin-Bialecki, A. The genus Psiadia: Review of traditional uses, phytochemistry and pharmacology. J. Ethnopharmacol., 2018, 210, 48-68.
[http://dx.doi.org/10.1016/j.jep.2017.08.023] [PMID: 28842341]
[91]
Orabi, K.Y.; Abaza, M.S.; Luqmani, Y.A.; Al-Attiyah, R. Psiadin and plectranthone selectively inhibit colorectal carcinoma cells proliferation via modulating cyclins signaling and apoptotic pathways. PLoS One, 2021, 16(6), e0252820.
[http://dx.doi.org/10.1371/journal.pone.0252820] [PMID: 34086816]
[92]
Varga, Z.V.; Ferdinandy, P.; Liaudet, L.; Pacher, P. Drug-induced mitochondrial dysfunction and cardiotoxicity. Am. J. Physiol. Heart Circ. Physiol., 2015, 309(9), H1453-H1467.
[http://dx.doi.org/10.1152/ajpheart.00554.2015] [PMID: 26386112]
[93]
Thappa, R.K.; Agarwal, S.G. Cymbopogon flexuosus oil a rich source of (+)-α-bisabolol. J. Essent. Oil Res., 1989, 1(3), 107-110.
[http://dx.doi.org/10.1080/10412905.1989.9697765]
[94]
Russell, K.; Jacob, S.E. Bisabolol. Dermatitis, 2010, 21(1), 57-58.
[http://dx.doi.org/10.2310/6620.2010.09072] [PMID: 20137740]
[95]
Cavalieri, E. Mariotto, S.; Fabrizi, C.; de Prati, A.C.; Gottardo, R.; Leone, S.; Berra, L.V.; Lauro, G.M.; Ciampa, A.R.; Suzuki, H. α-Bisabolol, a nontoxic natural compound, strongly induces apoptosis in glioma cells. Biochem. Biophys. Res. Commun., 2004, 315(3), 589-594.
[http://dx.doi.org/10.1016/j.bbrc.2004.01.088] [PMID: 14975741]
[96]
Darra, E.; Abdel-Azeim, S.; Manara, A.; Shoji, K.; Maréchal, J.D.; Mariotto, S.; Cavalieri, E.; Perbellini, L.; Pizza, C.; Perahia, D.; Crimi, M.; Suzuki, H. Insight into the apoptosis-inducing action of α-bisabolol towards malignant tumor cells: Involvement of lipid rafts and Bid. Arch. Biochem. Biophys., 2008, 476(2), 113-123.
[http://dx.doi.org/10.1016/j.abb.2008.02.004] [PMID: 18291090]
[97]
Cavalieri, E.; Rigo, A.; Bonifacio, M.; Carcereri de Prati, A.; Guardalben, E.; Bergamini, C.; Fato, R.; Pizzolo, G.; Suzuki, H.; Vinante, F. Pro-apoptotic activity of α-bisabolol in preclinical models of primary human acute leukemia cells. J. Transl. Med., 2011, 9(1), 45.
[http://dx.doi.org/10.1186/1479-5876-9-45] [PMID: 21510902]
[98]
Bahorun, T.; Luximon-Ramma, A.; Crozier, A.; Aruoma, O.I. Total phenol, flavonoid, proanthocyanidin and Vitamin C levels and antioxidant activities of Mauritian vegetables. J. Sci. Food Agric., 2004, 84(12), 1553-1561.
[http://dx.doi.org/10.1002/jsfa.1820]
[99]
Middleton, E., Jr; Kandaswami, C.; Theoharides, T.C. The effects of plant flavonoids on mammalian cells: Implications for inflammation, heart disease, and cancer. Pharmacol. Rev., 2000, 52(4), 673-751.
[PMID: 11121513]
[100]
Soobrattee, M.A.; Neergheen, V.S.; Luximon-Ramma, A.; Aruoma, O.I.; Bahorun, T. Phenolics as potential antioxidant therapeutic agents: Mechanism and actions. Mutat. Res., 2005, 579(1-2), 200-213.
[http://dx.doi.org/10.1016/j.mrfmmm.2005.03.023] [PMID: 16126236]
[101]
Gupta, S.C.; Patchva, S.; Aggarwal, B.B. Therapeutic roles of curcumin: Lessons learned from clinical trials. AAPS J., 2013, 15(1), 195-218.
[http://dx.doi.org/10.1208/s12248-012-9432-8] [PMID: 23143785]
[102]
Aggarwal, B.B.; Kumar, A.; Bharti, A.C. Anticancer potential of curcumin: Preclinical and clinical studies. Anticancer Res., 2003, 23(1A), 363-398.
[PMID: 12680238]
[103]
Vera-Ramirez, L.; Pérez-Lopez, P.; Varela-Lopez, A.; Ramirez-Tortosa, M.; Battino, M.; Quiles, J.L. Curcumin and liver disease. Biofactors, 2013, 39(1), 88-100.
[http://dx.doi.org/10.1002/biof.1057] [PMID: 23303639]
[104]
Wright, L.E.; Frye, J.B.; Gorti, B.; Timmermann, B.N.; Funk, J.L. Bioactivity of turmeric-derived curcuminoids and related metabolites in breast cancer. Curr. Pharm. Des., 2013, 19(34), 6218-6225.
[http://dx.doi.org/10.2174/1381612811319340013] [PMID: 23448448]
[105]
Hewlings, S.J.; Kalman, D.S. Curcumin: A review of its effects on human health. Foods, 2017, 6(10), 92.
[http://dx.doi.org/10.3390/foods6100092] [PMID: 29065496]
[106]
Kuo, M.L.; Huang, T.S.; Lin, J.K. Curcumin, an antioxidant and anti-tumor promoter, induces apoptosis in human leukemia cells. Biochim. Biophys. Acta, 1996, 1317(2), 95-100.
[http://dx.doi.org/10.1016/S0925-4439(96)00032-4] [PMID: 8950193]
[107]
Shi, M.; Cai, Q.; Yao, L.; Mao, Y.; Ming, Y.; Ouyang, G. Antiproliferation and apoptosis induced by curcumin in human ovarian cancer cells. Cell Biol. Int., 2006, 30(3), 221-226.
[http://dx.doi.org/10.1016/j.cellbi.2005.10.024] [PMID: 16376585]
[108]
Choudhuri, T.; Pal, S.; Agwarwal, M.L.; Das, T.; Sa, G. Curcumin induces apoptosis in human breast cancer cells through p53-dependent Bax induction. FEBS Lett., 2002, 512(1-3), 334-340.
[http://dx.doi.org/10.1016/S0014-5793(02)02292-5] [PMID: 11852106]
[109]
Radhakrishna Pillai, G.; Srivastava, A.S.; Hassanein, T.I.; Chauhan, D.P.; Carrier, E. Induction of apoptosis in human lung cancer cells by curcumin. Cancer Lett., 2004, 208(2), 163-170.
[http://dx.doi.org/10.1016/j.canlet.2004.01.008] [PMID: 15142674]
[110]
Karunagaran, D.; Rashmi, R.; Kumar, T.R. Induction of apoptosis by curcumin and its implications for cancer therapy. Curr. Cancer Drug Targets, 2005, 5(2), 117-129.
[http://dx.doi.org/10.2174/1568009053202081] [PMID: 15810876]
[111]
Srivastava, S.; Somasagara, R.R.; Hegde, M.; Nishana, M.; Tadi, S.K.; Srivastava, M.; Choudhary, B.; Raghavan, S.C. Quercetin, a natural flavonoid interacts with DNA, arrests cell cycle and causes tumor regression by activating mitochondrial pathway of apoptosis. Sci. Rep., 2016, 6(1), 24049.
[http://dx.doi.org/10.1038/srep24049] [PMID: 27068577]
[112]
Wei, Y.Q.; Zhao, X.; Kariya, Y.; Fukata, H.; Teshigawara, K.; Uchida, A. Induction of apoptosis by quercetin: Involvement of heat shock protein. Cancer Res., 1994, 54(18), 4952-4957.
[PMID: 8069862]
[113]
Tang, S.M.; Deng, X.T.; Zhou, J.; Li, Q.P.; Ge, X.X.; Miao, L. Pharmacological basis and new insights of quercetin action in respect to its anti-cancer effects. Biomed. Pharmacother., 2020, 121, 109604.
[http://dx.doi.org/10.1016/j.biopha.2019.109604] [PMID: 31733570]
[114]
He, F.; Pan, Q.H.; Shi, Y.; Duan, C.Q. Biosynthesis and genetic regulation of proanthocyanidins in plants. Molecules, 2008, 13(10), 2674-2703.
[http://dx.doi.org/10.3390/molecules13102674] [PMID: 18971863]
[115]
Bagchi, D.; Sen, C.K.; Ray, S.D.; Das, D.K.; Bagchi, M.; Preuss, H.G.; Vinson, J.A. Molecular mechanisms of cardioprotection by a novel grape seed proanthocyanidin extract. Mutat. Res., 2003, 523-524, 87-97.
[http://dx.doi.org/10.1016/S0027-5107(02)00324-X] [PMID: 12628506]
[116]
Kaur, M.; Singh, R.P.; Gu, M.; Agarwal, R.; Agarwal, C. Grape seed extract inhibits in vitro and in vivo growth of human colorectal carcinoma cells. Clin. Cancer Res., 2006, 12(20 Pt 1), 6194-6202.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-1465] [PMID: 17062697]
[117]
Bagchi, D.; Bagchi, M.; Stohs, S.J.; Das, D.K.; Ray, S.D.; Kuszynski, C.A.; Joshi, S.S.; Pruess, H.G. Free radicals and grape seed proanthocyanidin extract: Importance in human health and disease prevention. Toxicology, 2000, 148(2-3), 187-197.
[http://dx.doi.org/10.1016/S0300-483X(00)00210-9] [PMID: 10962138]