Generic placeholder image

Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1573-4064
ISSN (Online): 1875-6638

Research Article

Elucidating Molecular Interactions of Ten Natural Compounds Targeting E6 HPV High Risk Oncoproteins Using Microsecond Molecular Dynamics Simulations

Author(s): Thuluz Meza-Menchaca, Marcela Lizano-Soberón, Angel Trigos, Rossana C. Zepeda, Manuel E. Medina and Rodrigo Galindo-Murillo*

Volume 17, Issue 6, 2021

Published on: 29 January, 2020

Page: [587 - 600] Pages: 14

DOI: 10.2174/1573406416666200129145733

Price: $65

Abstract

Background: Cervical cancer is a major public health issue worldwide, occurring in the vast majority of cases (85%) in low-income countries. Human papillomavirus (HPV) mainly infects the mucosal epithelium, and a small portion causes over 600,000 cases every year worldwide at various anatomical spots, mainly leading to anogenital and head and neck.

Introduction: The E6 oncoprotein encoded by cancer-associated alpha HPV can transform epithelial cells into tumorigenic tissue. Therapy for this infection and blocking of the HPV E6 oncoprotein could be provided with cost-effective and abundant natural products which are an exponentially growing topic in the literature. Finding an active natural compound that readily blocks HPV E6 oncoprotein which could be available for developing countries without expensive extraction processes or costly synthetic pathways is of major interest.

Methods: Molecular dynamics simulation was performed using the most up-to-date AMBER protein force field ff14SB and a GPU enabled high performance computing cluster.

Results: In this research, we present a study of the binding properties between 10 selected natural compounds that are readily available with two variants of the E6 oncoprotein types (HPV-16 and HPV-18) using 10+ microsecond molecular dynamics simulations.

Conclusion: Our results suggest that crocetin, ergosterol peroxide and κ-carrageenan natural products bind strongly to both HPV-16 and HPV-18 and could potentially serve as a scaffolding for further drug development.

Keywords: HPV, E6, AMBER, cervical cancer, natural compounds, mucosal epithelium.

Graphical Abstract

[1]
Muñoz, N.; Bosch, F.X.; de Sanjosé, S.; Herrero, R.; Castellsagué, X.; Shah, K.V.; Snijders, P.J.; Meijer, C.J. International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med., 2003, 348(6), 518-527.
[http://dx.doi.org/10.1056/NEJMoa021641] [PMID: 12571259]
[2]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[3]
Pietsch, E.C.; Murphy, M.E. Low risk HPV-E6 traps p53 in the cytoplasm and induces p53-dependent apoptosis. Cancer Biol. Ther., 2008, 7(12), 1916-1918.
[http://dx.doi.org/10.4161/cbt.7.12.7169] [PMID: 19158479]
[4]
Gupta, S.; Kumar, P.; Das, B.C. HPV: Molecular pathways and targets. Curr. Probl. Cancer, 2018, 42(2), 161-174.
[http://dx.doi.org/10.1016/j.currproblcancer.2018.03.003] [PMID: 29706467]
[5]
Helt, A-M.; Galloway, D.A. Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis, 2003, 24(2), 159-169.
[http://dx.doi.org/10.1093/carcin/24.2.159] [PMID: 12584163]
[6]
Scheffner, M.; Werness, B.A.; Huibregtse, J.M.; Levine, A.J.; Howley, P.M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell, 1990, 63(6), 1129-1136.
[http://dx.doi.org/10.1016/0092-8674(90)90409-8] [PMID: 2175676]
[7]
Scheffner, M.; Huibregtse, J.M.; Vierstra, R.D.; Howley, P.M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell, 1993, 75(3), 495-505.
[http://dx.doi.org/10.1016/0092-8674(93)90384-3] [PMID: 8221889]
[8]
Lechner, M.S.; Mack, D.H.; Finicle, A.B.; Crook, T.; Vousden, K.H.; Laimins, L.A. Human papillomavirus E6 proteins bind p53 in vivo and abrogate p53-mediated repression of transcription. EMBO J., 1992, 11(8), 3045-3052.
[http://dx.doi.org/10.1002/j.1460-2075.1992.tb05375.x] [PMID: 1379175]
[9]
Mietz, J.A.; Unger, T.; Huibregtse, J.M.; Howley, P.M. The transcriptional transactivation function of wild-type p53 is inhibited by SV40 large T-antigen and by HPV-16 E6 oncoprotein. EMBO J., 1992, 11(13), 5013-5020.
[http://dx.doi.org/10.1002/j.1460-2075.1992.tb05608.x] [PMID: 1464323]
[10]
Jones, D.L.; Alani, R.M.; Münger, K. The human papillomavirus E7 oncoprotein can uncouple cellular differentiation and proliferation in human keratinocytes by abrogating p21Cip1-mediated inhibition of cdk2. Genes Dev., 1997, 11(16), 2101-2111.
[http://dx.doi.org/10.1101/gad.11.16.2101] [PMID: 9284049]
[11]
Klingelhutz, A.J.; Foster, S.A.; McDougall, J.K. Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature, 1996, 380(6569), 79-82.
[http://dx.doi.org/10.1038/380079a0] [PMID: 8598912]
[12]
Gewin, L.; Galloway, D.A. E box-dependent activation of telomerase by human papillomavirus type 16 E6 does not require induction of c-myc. J. Virol., 2001, 75(15), 7198-7201.
[http://dx.doi.org/10.1128/JVI.75.15.7198-7201.2001] [PMID: 11435602]
[13]
Oh, S.T.; Kyo, S.; Laimins, L.A. Telomerase activation by human papillomavirus type 16 E6 protein: induction of human telomerase reverse transcriptase expression through Myc and GC-rich Sp1 binding sites. J. Virol., 2001, 75(12), 5559-5566.
[http://dx.doi.org/10.1128/JVI.75.12.5559-5566.2001] [PMID: 11356963]
[14]
Veldman, T.; Liu, X.; Yuan, H.; Schlegel, R. Human papillomavirus E6 and Myc proteins associate in vivo and bind to and cooperatively activate the telomerase reverse transcriptase promoter. Proc. Natl. Acad. Sci. USA, 2003, 100(14), 8211-8216.
[http://dx.doi.org/10.1073/pnas.1435900100] [PMID: 12821782]
[15]
Efferth, T. In From ancient herb to modern drug: Artemisia annua and artemisinin for cancer therapy Sem. Can. Biol; Elsevier, 2017, pp. 65-83.
[16]
Cuzzocrea, S.; Mazzon, E.; Dugo, L.; Serraino, I.; Ciccolo, A.; Centorrino, T.; De Sarro, A.; Caputi, A.P. Protective effects of n-acetylcysteine on lung injury and red blood cell modification induced by carrageenan in the rat. FASEB J., 2001, 15(7), 1187-1200.
[http://dx.doi.org/10.1096/fj.00-0526hyp] [PMID: 11344087]
[17]
Ben-Chetrit, E.; Levy, M. Familial Mediterranean fever. Lancet, 1998, 351(9103), 659-664.
[http://dx.doi.org/10.1016/S0140-6736(97)09408-7] [PMID: 9500348]
[18]
Pal, H.C.; Prasad, R.; Katiyar, S.K. Cryptolepine inhibits melanoma cell growth through coordinated changes in mitochondrial biogenesis, dynamics and metabolic tumor suppressor AMPKα1/2-LKB1. Sci. Rep., 2017, 7(1), 1498.
[http://dx.doi.org/10.1038/s41598-017-01659-7] [PMID: 28473727]
[19]
Gu, S.; He, J. Daphnoretin induces cell cycle arrest and apoptosis in human osteosarcoma (HOS) cells. Molecules, 2012, 17(1), 598-612.
[http://dx.doi.org/10.3390/molecules17010598] [PMID: 22231496]
[20]
Garbett, N.C.; Graves, D.E. Extending nature’s leads: the anticancer agent ellipticine. Curr. Med. Chem. Anticancer Agents, 2004, 4(2), 149-172.
[http://dx.doi.org/10.2174/1568011043482070] [PMID: 15032720]
[21]
Zhong, Y.; Shahidi, F. Lipophilized epigallocatechin gallate (EGCG) derivatives as novel antioxidants. J. Agric. Food Chem., 2011, 59(12), 6526-6533.
[http://dx.doi.org/10.1021/jf201050j] [PMID: 21526762]
[22]
Meza-Menchaca, T.; Suárez-Medellín, J.; Del Ángel-Piña, C.; Trigos, Á. The amoebicidal effect of ergosterol peroxide isolated from Pleurotus ostreatus. Phytother. Res., 2015, 29(12), 1982-1986.
[http://dx.doi.org/10.1002/ptr.5474] [PMID: 26392373]
[23]
Carpenter, J.E. Extension of Lewis structure concepts to open-shell and excited- state molecular species. PhD Thesis. University of Wisconsin, . 1987.
[24]
Biasini, M.; Bienert, S.; Waterhouse, A.; Arnold, K.; Studer, G.; Schmidt, T.; Kiefer, F.; Gallo Cassarino, T.; Bertoni, M.; Bordoli, L.; Schwede, T. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information., Nucleic Acids Res, 2014, 42 ((Web Server issue)), W252-8...
[http://dx.doi.org/10.1093/nar/gku340]
[25]
Katoh, K.; Misawa, K.; Kuma, K.; Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res., 2002, 30(14), 3059-3066.
[http://dx.doi.org/10.1093/nar/gkf436] [PMID: 12136088]
[26]
Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol., 2018, 35(6), 1547-1549.
[http://dx.doi.org/10.1093/molbev/msy096] [PMID: 29722887]
[27]
Wiederstein, M.; Sippl, M.J. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins., Nucleic Acids Res., 2007, 35(Web Server issue)W407-10..
[http://dx.doi.org/10.1093/nar/gkm290] [PMID: 17517781]
[28]
Allen, W.J.; Fochtman, B.C.; Balius, T.E.; Rizzo, R.C. Customizable de novo design strategies for DOCK: Application to HIVgp41 and other therapeutic targets. J. Comput. Chem., 2017, 38(30), 2641-2663.
[http://dx.doi.org/10.1002/jcc.25052] [PMID: 28940386]
[29]
Wang, J.; Wolf, R.M.; Caldwell, J.W.; Kollman, P.A.; Case, D.A. Development and testing of a general amber force field. J. Comput. Chem., 2004, 25(9), 1157-1174.
[http://dx.doi.org/10.1002/jcc.20035] [PMID: 15116359]
[30]
Maier, J.A.; Martinez, C.; Kasavajhala, K.; Wickstrom, L.; Hauser, K.E.; Simmerling, C. ff14SB: improving the accuracy of protein side chain and backbone parameters from ff99SB. J. Chem. Theory Comput., 2015, 11(8), 3696-3713.
[http://dx.doi.org/10.1021/acs.jctc.5b00255] [PMID: 26574453]
[31]
Peters, M.B.; Yang, Y.; Wang, B.; Füsti-Molnár, L.; Weaver, M.N.; Merz, K.M. Jr Structural survey of zinc-containing proteins and development of the zinc AMBER force field (ZAFF). J. Chem. Theory Comput., 2010, 6(9), 2935-2947.
[http://dx.doi.org/10.1021/ct1002626] [PMID: 20856692]
[32]
Jorgensen, W.L.; Chandrasekhar, J.; Madura, J.; Impey, R.W.; Klein, M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 1983, 79, 926-935.
[http://dx.doi.org/10.1063/1.445869]
[33]
Joung, I.S.; Cheatham, T.E., III Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J. Phys. Chem. B, 2008, 112(30), 9020-9041.
[http://dx.doi.org/10.1021/jp8001614] [PMID: 18593145]
[34]
Ryckaert, J-P.; Ciccotti, G.; Berendsen, H.J. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys., 1977, 23, 327-341.
[http://dx.doi.org/10.1016/0021-9991(77)90098-5]
[35]
Roe, D.R.; Cheatham, T.E. III PTRAJ and CPPTRAJ: software for processing and analysis of molecular dynamics trajectory data. J. Chem. Theory Comput., 2013, 9(7), 3084-3095.
[http://dx.doi.org/10.1021/ct400341p] [PMID: 26583988]
[36]
Roe, D.R.; Cheatham, T.E. III Parallelization of CPPTRAJ enables large scale analysis of molecular dynamics trajectory data. J. Comput. Chem., 2018, 39(25), 2110-2117.
[http://dx.doi.org/10.1002/jcc.25382] [PMID: 30368859]
[37]
Miller, B.R., III; McGee, T.D., Jr; Swails, J.M.; Homeyer, N.; Gohlke, H.; Roitberg, A.E. MMPBSA. py: an efficient program for end-state free energy calculations. J. Chem. Theory Comput., 2012, 8(9), 3314-3321.
[http://dx.doi.org/10.1021/ct300418h] [PMID: 26605738]
[38]
Onufriev, A.; Bashford, D.; Case, D.A. Exploring protein native states and large-scale conformational changes with a modified generalized born model. Proteins, 2004, 55(2), 383-394.
[http://dx.doi.org/10.1002/prot.20033] [PMID: 15048829]
[39]
Stierand, K.; Maass, P.C.; Rarey, M. Molecular complexes at a glance: automated generation of two-dimensional complex diagrams. Bioinformatics, 2006, 22(14), 1710-1716.
[http://dx.doi.org/10.1093/bioinformatics/btl150] [PMID: 16632493]
[40]
Stierand, K.; Rarey, M. From modeling to medicinal chemistry: automatic generation of two-dimensional complex diagrams. ChemMedChem, 2007, 2(6), 853-860.
[http://dx.doi.org/10.1002/cmdc.200700010] [PMID: 17436259]
[41]
Salomon‐Ferrer, R.; Case, D.A.; Walker, R.C. An overview of the Amber biomolecular simulation package. Wiley Interdiscip. Rev. Comput. Mol. Sci., 2013, 3, 198-210.
[http://dx.doi.org/10.1002/wcms.1121]
[42]
Woerdenbag, H.J.; Moskal, T.A.; Pras, N.; Malingré, T.M.; el-Feraly, F.S.; Kampinga, H.H.; Konings, A.W. Cytotoxicity of artemisinin-related endoperoxides to Ehrlich ascites tumor cells. J. Nat. Prod., 1993, 56(6), 849-856.
[http://dx.doi.org/10.1021/np50096a007] [PMID: 8350087]
[43]
Zhang, Y.J.; Gallis, B.; Taya, M.; Wang, S.; Ho, R.J.; Sasaki, T. pH-responsive artemisinin derivatives and lipid nanoparticle formulations inhibit growth of breast cancer cells in vitro and induce down-regulation of HER family members. PLoS One, 2013, 8(3), e59086.
[http://dx.doi.org/10.1371/journal.pone.0059086] [PMID: 23516601]
[44]
Chen, H.H.; Zhou, H.J.; Wang, W.Q.; Wu, G.D. Antimalarial dihydroartemisinin also inhibits angiogenesis. Cancer Chemother. Pharmacol., 2004, 53(5), 423-432.
[http://dx.doi.org/10.1007/s00280-003-0751-4] [PMID: 15132130]
[45]
Paeshuyse, J.; Coelmont, L.; Vliegen, I. Van hemel, J.; Vandenkerckhove, J.; Peys, E.; Sas, B.; De Clercq, E.; Neyts, J. Hemin potentiates the anti-hepatitis C virus activity of the antimalarial drug artemisinin. Biochem. Biophys. Res. Commun., 2006, 348(1), 139-144.
[http://dx.doi.org/10.1016/j.bbrc.2006.07.014] [PMID: 16875675]
[46]
Merali, S.; Meshnick, S.R. Susceptibility of Pneumocystis carinii to artemisinin in vitro. Antimicrob. Agents Chemother., 1991, 35(6), 1225-1227.
[http://dx.doi.org/10.1128/AAC.35.6.1225] [PMID: 1929266]
[47]
Xu, H.; He, Y.; Yang, X.; Liang, L.; Zhan, Z.; Ye, Y.; Yang, X.; Lian, F.; Sun, L. Anti-malarial agent artesunate inhibits TNF-α-induced production of proinflammatory cytokines via inhibition of NF-kappaB and PI3 kinase/Akt signal pathway in human rheumatoid arthritis fibroblast-like synoviocytes. Rheumatology (Oxford), 2007, 46(6), 920-926.
[http://dx.doi.org/10.1093/rheumatology/kem014] [PMID: 17314215]
[48]
Razavi, A.; Nouri, H.R.; Mehrabian, F.; Mirshafiey, A. Treatment of experimental nephrotic syndrome with artesunate. Int. J. Toxicol., 2007, 26(4), 373-380.
[http://dx.doi.org/10.1080/10915810701493293] [PMID: 17661229]
[49]
Zhao, M.; Xue, D-B.; Zheng, B.; Zhang, W-H.; Pan, S-H.; Sun, B. Induction of apoptosis by artemisinin relieving the severity of inflammation in caerulein-induced acute pancreatitis. World J. Gastroenterol., 2007, 13(42), 5612-5617.
[http://dx.doi.org/10.3748/wjg.v13.i42.5612] [PMID: 17948936]
[50]
Li, W.D.; Dong, Y.J.; Tu, Y.Y.; Lin, Z.B. Dihydroarteannuin ameliorates lupus symptom of BXSB mice by inhibiting production of TNF-alpha and blocking the signaling pathway NF-kappa B translocation. Int. Immunopharmacol., 2006, 6(8), 1243-1250.
[http://dx.doi.org/10.1016/j.intimp.2006.03.004] [PMID: 16782536]
[51]
Majcher, U.; Klejborowska, G.; Kaik, M.; Maj, E.; Wietrzyk, J.; Moshari, M.; Preto, J.; Tuszynski, J.A.; Huczyński, A. Synthesis and Biological Evaluation of Novel Triple-Modified Colchicine Derivatives as Potent Tubulin-Targeting Anticancer Agents. Cells, 2018, 7(11), 216.
[http://dx.doi.org/10.3390/cells7110216] [PMID: 30463236]
[52]
Ben-Chetrit, E.; Bergmann, S.; Sood, R. Mechanism of the anti-inflammatory effect of colchicine in rheumatic diseases: a possible new outlook through microarray analysis. Rheumatology (Oxford), 2006, 45(3), 274-282.
[http://dx.doi.org/10.1093/rheumatology/kei140] [PMID: 16188942]
[53]
Wortmann, R.L.; Macdonald, P.A.; Hunt, B.; Jackson, R.L. Effect of prophylaxis on gout flares after the initiation of urate-lowering therapy: analysis of data from three phase III trials. Clin. Ther., 2010, 32(14), 2386-2397.
[http://dx.doi.org/10.1016/j.clinthera.2011.01.008] [PMID: 21353107]
[54]
Ray, P.; Guha, D.; Chakraborty, J.; Banerjee, S.; Adhikary, A.; Chakraborty, S.; Das, T.; Sa, G. Crocetin exploits p53-induced death domain (PIDD) and FAS-associated death domain (FADD) proteins to induce apoptosis in colorectal cancer. Sci. Rep., 2016, 6, 32979.
[http://dx.doi.org/10.1038/srep32979] [PMID: 27622714]
[55]
Kanakis, C.D.; Tarantilis, P.A.; Tajmir-Riahi, H.A.; Polissiou, M.G. Crocetin, dimethylcrocetin, and safranal bind human serum albumin: stability and antioxidative properties. J. Agric. Food Chem., 2007, 55(3), 970-977.
[http://dx.doi.org/10.1021/jf062638l] [PMID: 17263501]
[56]
Aung, H.H.; Wang, C.Z.; Ni, M.; Fishbein, A.; Mehendale, S.R.; Xie, J.T.; Shoyama, C.Y.; Yuan, C.S. Crocin from Crocus sativus possesses significant anti-proliferation effects on human colorectal cancer cells. Exp. Oncol., 2007, 29(3), 175-180.
[PMID: 18004240]
[57]
Sheng, L.; Qian, Z.; Zheng, S.; Xi, L. Mechanism of hypolipidemic effect of crocin in rats: crocin inhibits pancreatic lipase. Eur. J. Pharmacol., 2006, 543(1-3), 116-122.
[http://dx.doi.org/10.1016/j.ejphar.2006.05.038] [PMID: 16828739]
[58]
Lisgarten, J.N.; Coll, M.; Portugal, J.; Wright, C.W.; Aymami, J. The antimalarial and cytotoxic drug cryptolepine intercalates into DNA at cytosine-cytosine sites. Nat. Struct. Biol., 2002, 9(1), 57-60.
[http://dx.doi.org/10.1038/nsb729] [PMID: 11731803]
[59]
Olajide, O.A.; Bhatia, H.S.; de Oliveira, A.C.; Wright, C.W.; Fiebich, B.L. Anti-neuroinflammatory properties of synthetic cryptolepine in human neuroblastoma cells: possible involvement of NF-κB and p38 MAPK inhibition. Eur. J. Med. Chem., 2013, 63, 333-339.
[http://dx.doi.org/10.1016/j.ejmech.2013.02.004] [PMID: 23507189]
[60]
Oluwafemi, A.J.; Okanla, E.O.; Camps, P.; Muñoz-Torrerob, D.; Mackey, Z.B.; Chiang, P.K.; Seville, S.; Wright, C.W. Evaluation of cryptolepine and huperzine derivatives as lead compounds towards new agents for the treatment of human African trypanosomiasis. Nat. Prod. Commun., 2009, 4(2), 193-198.
[http://dx.doi.org/10.1177/1934578X0900400205] [PMID: 19370921]
[61]
Jonckers, T.H.; van Miert, S.; Cimanga, K.; Bailly, C.; Colson, P.; De Pauw-Gillet, M-C.; van den Heuvel, H.; Claeys, M.; Lemière, F.; Esmans, E.L.; Rozenski, J.; Quirijnen, L.; Maes, L.; Dommisse, R.; Lemière, G.L.; Vlietinck, A.; Pieters, L. Synthesis, cytotoxicity, and antiplasmodial and antitrypanosomal activity of new neocryptolepine derivatives. J. Med. Chem., 2002, 45(16), 3497-3508.
[http://dx.doi.org/10.1021/jm011102i] [PMID: 12139461]
[62]
Ansah, C.; Mensah, K.B. A review of the anticancer potential of the antimalarial herbal cryptolepis sanguinolenta and its major alkaloid cryptolepine. Ghana Med. J., 2013, 47(3), 137-147.
[PMID: 24391229]
[63]
Jiang, H.F.; Wu, Z.; Bai, X.; Zhang, Y.; He, P. Effect of daphnoretin on the proliferation and apoptosis of A549 lung cancer cells in vitro. Oncol. Lett., 2014, 8(3), 1139-1142.
[http://dx.doi.org/10.3892/ol.2014.2296] [PMID: 25120673]
[64]
Ho, W.S.; Xue, J.Y.; Sun, S.S.; Ooi, V.E.; Li, Y.L. Antiviral activity of daphnoretin isolated from Wikstroemia indica. Phytother. Res., 2010, 24(5), 657-661.
[PMID: 19610034]
[65]
Diogo, C.V.; Félix, L.; Vilela, S.; Burgeiro, A.; Barbosa, I.A.; Carvalho, M.J.; Oliveira, P.J.; Peixoto, F.P. Mitochondrial toxicity of the phyotochemicals daphnetoxin and daphnoretin--relevance for possible anti-cancer application. Toxicol. In Vitro, 2009, 23(5), 772-779.
[http://dx.doi.org/10.1016/j.tiv.2009.04.002] [PMID: 19362137]
[66]
Lichota, A.; Gwozdzinski, K. Anticancer Activity of Natural Compounds from Plant and Marine Environment. Int. J. Mol. Sci., 2018, 19(11), 3533.
[http://dx.doi.org/10.3390/ijms19113533] [PMID: 30423952]
[67]
Wen, H.L.; Yang, G.; Dong, Q.R. Ellipticine inhibits the proliferation and induces apoptosis in rheumatoid arthritis fibroblast-like synoviocytes via the STAT3 pathway. Immunopharmacol. Immunotoxicol., 2017, 39(4), 219-224.
[http://dx.doi.org/10.1080/08923973.2017.1327963] [PMID: 28555524]
[68]
Watamoto, T.; Egusa, H.; Sawase, T.; Yatani, H. Screening of pharmacologically active small molecule compounds identifies antifungal agents against Candida biofilms. Front. Microbiol., 2015, 6, 1453.
[http://dx.doi.org/10.3389/fmicb.2015.01453] [PMID: 26733987]
[69]
Montoia, A.; Rocha, E.; Silva, L.F.; Torres, Z.E.; Costa, D.S.; Henrique, M.C.; Lima, E.S.; Vasconcellos, M.C.; Souza, R.C.; Costa, M.R.; Grafov, A.; Grafova, I.; Eberlin, M.N.; Tadei, W.P.; Amorim, R.C.; Pohlit, A.M. Antiplasmodial activity of synthetic ellipticine derivatives and an isolated analog. Bioorg. Med. Chem. Lett., 2014, 24(12), 2631-2634.
[http://dx.doi.org/10.1016/j.bmcl.2014.04.070] [PMID: 24813729]
[70]
Schröder, L.; Marahrens, P.; Koch, J.G.; Heidegger, H.; Vilsmeier, T.; Phan-Brehm, T.; Hofmann, S.; Mahner, S.; Jeschke, U.; Richter, D.U. Effects of green tea, matcha tea and their components epigallocatechin gallate and quercetin on MCF 7 and MDA-MB-231 breast carcinoma cells. Oncol. Rep., 2019, 41(1), 387-396.
[PMID: 30320348]
[71]
Peixoto-Neves, D.; Soni, H.; Adebiyi, A. CGRPergic Nerve TRPA1 Channels Contribute to Epigallocatechin Gallate-Induced Neurogenic Vasodilation. ACS Chem. Neurosci., 2019, 10(1), 216-220.
[http://dx.doi.org/10.1021/acschemneuro.8b00493] [PMID: 30513192]
[72]
Lee, S.; Razqan, G.S.; Kwon, D.H. Antibacterial activity of epigallocatechin-3-gallate (EGCG) and its synergism with β-lactam antibiotics sensitizing carbapenem-associated multidrug resistant clinical isolates of Acinetobacter baumannii. Phytomedicine, 2017, 24, 49-55.
[http://dx.doi.org/10.1016/j.phymed.2016.11.007] [PMID: 28160861]
[73]
Ma, L.; Chen, H.; Dong, P.; Lu, X. Anti-inflammatory and anticancer activities of extracts and compounds from the mushroom Inonotus obliquus. Food Chem., 2013, 139(1-4), 503-508.
[http://dx.doi.org/10.1016/j.foodchem.2013.01.030] [PMID: 23561137]
[74]
Lindequist, U.; Lesnau, A.; Teuscher, E.; Pilgrim, H. [The antiviral action of ergosterol peroxide] Pharmazie, 1989, 44(8), 579-580.
[PMID: 2594833]
[75]
Ding, Y.Y.; Liu, F.; Shi, C.; Zhang, Y.; Li, N. [Chemical constituents from Phellinus igniarius and their anti-tumor activity in vitro] Zhongguo Zhongyao Zazhi, 2016, 41(16), 3042-3048.
[PMID: 28920346]
[76]
Bernard, M.M.; McConnery, J.R.; Hoskin, D.W. [10]-Gingerol, a major phenolic constituent of ginger root, induces cell cycle arrest and apoptosis in triple-negative breast cancer cells. Exp. Mol. Pathol., 2017, 102(2), 370-376.
[http://dx.doi.org/10.1016/j.yexmp.2017.03.006] [PMID: 28315687]
[77]
Zhang, F.; Thakur, K.; Hu, F.; Zhang, J.G.; Wei, Z.J. Cross-talk between 10-gingerol and its anti-cancerous potential: a recent update. Food Funct., 2017, 8(8), 2635-2649.
[http://dx.doi.org/10.1039/C7FO00844A] [PMID: 28745358]
[78]
Kapoor, V.; Aggarwal, S.; Das, S.N. 6‐Gingerol mediates its anti tumor activities in human oral and cervical cancer cell lines through apoptosis and cell cycle arrest. Phytother. Res., 2016, 30(4), 588-595.
[http://dx.doi.org/10.1002/ptr.5561] [PMID: 26749462]
[79]
Dugasani, S.; Pichika, M.R.; Nadarajah, V.D.; Balijepalli, M.K.; Tandra, S.; Korlakunta, J.N. Comparative antioxidant and anti-inflammatory effects of [6]-gingerol, [8]-gingerol, [10]-gingerol and [6]-shogaol. J. Ethnopharmacol., 2010, 127(2), 515-520.
[http://dx.doi.org/10.1016/j.jep.2009.10.004] [PMID: 19833188]
[80]
Koenighofer, M.; Lion, T.; Bodenteich, A.; Prieschl-Grassauer, E.; Grassauer, A.; Unger, H.; Mueller, C.A.; Fazekas, T. Carrageenan nasal spray in virus confirmed common cold: individual patient data analysis of two randomized controlled trials. Multidiscip. Respir. Med., 2014, 9(1), 57.
[http://dx.doi.org/10.1186/2049-6958-9-57] [PMID: 25411637]
[81]
Sathuvan, M.; Thangam, R.; Gajendiran, M.; Vivek, R.; Balasubramanian, S.; Nagaraj, S.; Gunasekaran, P.; Madhan, B.; Rengasamy, R. κ-Carrageenan: An effective drug carrier to deliver curcumin in cancer cells and to induce apoptosis. Carbohydr. Polym., 2017, 160, 184-193.
[http://dx.doi.org/10.1016/j.carbpol.2016.12.049] [PMID: 28115093]
[82]
Duarte, D.B.; Vasko, M.R.; Fehrenbacher, J.C. Models of Inflammation: Carrageenan Air Pouch. Curr. Protocols Pharmacol., 2016, 72, 1-9, 9..
[http://dx.doi.org/10.1002/0471141755.ph0506s72] [PMID: 26995549]
[83]
El-Fawal, G. Preparation, characterization and antibacterial activity of biodegradable films prepared from carrageenan. J. Food Sci. Technol., 2014, 51(9), 2234-2239.
[http://dx.doi.org/10.1007/s13197-013-1255-9] [PMID: 25190889]
[84]
Rietz, A.; Petrov, D.P.; Bartolowits, M.; DeSmet, M.; Davisson, V.J.; Androphy, E.J. Molecular Probing of the HPV-16 E6 Protein Alpha Helix Binding Groove with Small Molecule Inhibitors. PLoS One, 2016, 11(2), e0149845.
[http://dx.doi.org/10.1371/journal.pone.0149845] [PMID: 26915086]
[85]
Zanier, K.; Charbonnier, S.; Sidi, A.O.; McEwen, A.G.; Ferrario, M.G.; Poussin-Courmontagne, P.; Cura, V.; Brimer, N.; Babah, K.O.; Ansari, T.; Muller, I.; Stote, R.H.; Cavarelli, J.; Vande Pol, S.; Travé, G. Structural basis for hijacking of cellular LxxLL motifs by papillomavirus E6 oncoproteins. Science, 2013, 339(6120), 694-698.
[http://dx.doi.org/10.1126/science.1229934] [PMID: 23393263]
[86]
Shah, M.; Anwar, M.A.; Park, S.; Jafri, S.S.; Choi, S. In silico mechanistic analysis of IRF3 inactivation and high-risk HPV E6 species-dependent drug response. Sci. Rep., 2015, 5, 13446.
[http://dx.doi.org/10.1038/srep13446] [PMID: 26289783]
[87]
Buck, C.B.; Thompson, C.D.; Roberts, J.N.; Müller, M.; Lowy, D.R.; Schiller, J.T. Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog., 2006, 2(7), e69.
[http://dx.doi.org/10.1371/journal.ppat.0020069] [PMID: 16839203]

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