Molecular Docking Study, Cytotoxicity, Cell Cycle Arrest and Apoptotic Induction of Novel Chalcones Incorporating Thiadiazolyl Isoquinoline in Cervical Cancer

Author(s): Mohamed A. Tantawy, Farid M. Sroor*, Magda F. Mohamed*, Mostafa E. El-Naggar, Fatma M. Saleh, Hamdi M. Hassaneen, Ismail A. Abdelhamid*

Journal Name: Anti-Cancer Agents in Medicinal Chemistry
(Formerly Current Medicinal Chemistry - Anti-Cancer Agents)

Volume 20 , Issue 1 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Chalcones are naturally occurring compounds found in various plant species which are widely used for the traditional popular treatments. Chalcones are distinguished secondary metabolites that are reported to display diverse biological activities such as antiviral, antiplatelet, anti-inflammatory, anticancer, antibacterial and antioxidant agents. The presence of a,ß-unsaturated carbonyl group in chalcones is assumed to be responsible for their bioactivity. In addition, heterocyclic compounds having nitrogen such as isoquinolines are of considerable interest as they constitute the core structural element of many alkaloids that have enormous pharmacological activities.

Objective: The objective of this study is the synthesis and biological activity of novel chalcones incorporating thiadiazolyl isoquinoline as potential anticancer candidates. Different genetic tools were used in an attempt to know the mechanism of action of this compound against breast cancer.

Methods: An efficient one pot synthesis of novel chalcones incorporating thiadiazolyl isoquinoline has been developed. The cytotoxic activity of the novel synthesized compounds was performed against four different kinds of cancer cell lines.

Results: Among all the tested derivatives, chalcone 3 has the best cytotoxic profile against A549, MCF7, and HeLa cell lines, with IC50s (66.1, 51.3, and 85.1μM, respectively). Molecular docking studies for chalcone 3 revealed that CDK2, and EGFRTK domains have strong binding affinities toward the novel chalcone 3, while tubulin-colchicine-ustiloxin, and VEGFRTK domains illustrated moderate mode of binding.

Conclusion: We have developed an efficient method for the synthesis of novel chalcones incorporating thiadiazolyl isoquinoline. All compounds showed better cytotoxicity results against four kinds of cancer cell lines (A549, MCF7, HCT116, and HELA cells). The results depicted that chalcone 3 has a high and promising cytotoxic effect against HELA cell line and the mechanism of cytotoxicity was widely studied through different theoretical and experimental tools. Thus, the newly synthesized derivative 3 can be utilized as a novel chemotherapeutic compound for cervical carcinoma.

Keywords: Chalcones, synthesis, cervical cancer, molecular docking, apoptosis, cell cycle arrest, DNA fragmentation, ELISA.

[1]
Chavan, B.B.; Gadekar, A.S.; Mehta, P.P.; Vawhal, P.K.; Kolsure, A.K.; Chabukswar, A.R. Synthesis and medicinal significance of chalcones-A review. Asian J. Biomed. Pharm. Sci., 2015, 13(1), 459-500.
[2]
Huang, L.; Nikolic, D.; van Breemen, R.B. Hepatic metabolism of licochalcone A, a potential chemopreventive chalcone from licorice (Glycyrrhiza inflata), determined using liquid chromatography-tandem mass spectrometry. Anal. Bioanal. Chem., 2017, 409(30), 6937-6948.
[http://dx.doi.org/10.1007/s00216-017-0642-x] [PMID: 29127460]
[3]
Ohnogi, H.; Kudo, Y.; Tahara, K.; Sugiyama, K.; Enoki, T.; Hayami, S.; Sagawa, H.; Tanimura, Y.; Aoi, W.; Naito, Y.; Kato, I.; Yoshikawa, T. Six new chalcones from Angelica keiskei inducing adiponectin production in 3T3-L1 adipocytes. Biosci. Biotechnol. Biochem., 2012, 76(5), 961-966.
[http://dx.doi.org/10.1271/bbb.110976] [PMID: 22738967]
[4]
Ban, Z.; Qin, H.; Mitchell, A.J.; Liu, B.; Zhang, F.; Weng, J-K.; Dixon, R.A.; Wang, G. Noncatalytic chalcone isomerase-fold proteins in Humulus lupulus are auxiliary components in prenylated flavonoid biosynthesis. Proc. Natl. Acad. Sci. USA, 2018, 115(22), E5223-E5232.
[http://dx.doi.org/10.1073/pnas.1802223115] [PMID: 29760092]
[5]
Pang, Y.; Nikolic, D.; Zhu, D.; Chadwick, L.R.; Pauli, G.F.; Farnsworth, N.R.; van Breemen, R.B. Binding of the hop (Humulus lupulus L.) chalcone xanthohumol to cytosolic proteins in Caco-2 intestinal epithelial cells. Mol. Nutr. Food Res., 2007, 51(7), 872-879.
[http://dx.doi.org/10.1002/mnfr.200600252] [PMID: 17579893]
[6]
Lei, W.; Tang, S-H.; Luo, K-M.; Sun, M. Molecular cloning and expression profiling of a chalcone synthase gene from hairy root cultures of Scutellaria viscidula Bunge. Genet. Mol. Biol., 2010, 33(2), 285-291.
[http://dx.doi.org/10.1590/S1415-47572010005000031] [PMID: 21637484]
[7]
Lei, W.; Sun, M.; Luo, K.M.; Shui, X.R.; Sun, Y.M.; Tang, H. [Compute simulation to characterize structure and function of chalcone synthase from Scutellaria baicalensis Georgi]. Mol. Biol. (Mosk.), 2009, 43(6), 1082-1087.
[PMID: 20088386]
[8]
Zhou, Y.; Nagashima, S.; Hirotani, M.; Suzuki, H.; Yoshikawa, T. Expression of the chalcone synthase gene in Scutellaria baicalensis hairy root cultures was unusually reduced by environmental stresses. Plant Biotechnol., 2003, 20(3), 207-214.
[http://dx.doi.org/10.5511/plantbiotechnology.20.207]
[9]
Onyilagha, J.C.; Malhotra, B.; Elder, M.; French, C.J.; Towers, G.H.N. Comparative studies of inhibitory activities of chalcones on Tomato Ringspot Virus (ToRSV). Can. J. Plant Pathol., 1997, 19(2), 133-137.
[http://dx.doi.org/10.1080/07060669709500541]
[10]
Lin, C-N.; Hsieh, H-K.; Ko, H-H.; Hsu, M-F.; Lin, H-C.; Chang, Y-L.; Chung, M-I.; Kang, J-J.; Wang, J-P.; Teng, C-M. Chalcones as potent antiplatelet agents and calcium channel blockers. Drug Dev. Res., 2001, 53(1), 9-14.
[http://dx.doi.org/10.1002/ddr.1163]
[11]
Li, R.; Kenyon, G.L.; Cohen, F.E.; Chen, X.; Gong, B.; Dominguez, J.N.; Davidson, E.; Kurzban, G.; Miller, R.E.; Nuzum, E.O. In vitro antimalarial activity of chalcones and their derivatives. J. Med. Chem., 1995, 38(26), 5031-5037.
[http://dx.doi.org/10.1021/jm00026a010] [PMID: 8544179]
[12]
Hsieh, H-K.; Tsao, L-T.; Wang, J-P.; Lin, C-N. Synthesis and anti-inflammatory effect of chalcones. J. Pharm. Pharmacol., 2000, 52(2), 163-171.
[http://dx.doi.org/10.1211/0022357001773814] [PMID: 10714946]
[13]
Bandgar, B.P.; Gawande, S.S.; Bodade, R.G.; Gawande, N.M.; Khobragade, C.N. Synthesis and biological evaluation of a novel series of pyrazole chalcones as anti-inflammatory, antioxidant and antimicrobial agents. Bioorg. Med. Chem., 2009, 17(24), 8168-8173.
[http://dx.doi.org/10.1016/j.bmc.2009.10.035] [PMID: 19896853]
[14]
Bekhit, A.A.; Abdel-Aziem, T. Design, synthesis and biological evaluation of some pyrazole derivatives as anti-inflammatory-antimicrobial agents. Bioorg. Med. Chem., 2004, 12(8), 1935-1945.
[http://dx.doi.org/10.1016/j.bmc.2004.01.037] [PMID: 15051061]
[15]
Shenvi, S.; Kumar, K.; Hatti, K.S.; Rijesh, K.; Diwakar, L.; Reddy, G.C. Synthesis, anticancer and antioxidant activities of 2,4,5-trimethoxy chalcones and analogues from asaronaldehyde: structure-activity relationship. Eur. J. Med. Chem., 2013, 62, 435-442.
[http://dx.doi.org/10.1016/j.ejmech.2013.01.018] [PMID: 23395966]
[16]
Mohamed, M.F.; Mohamed, M.S.; Shouman, S.A.; Fathi, M.M.; Abdelhamid, I.A. Synthesis and biological evaluation of a novel series of chalcones incorporated pyrazole moiety as anticancer and antimicrobial agents. Appl. Biochem. Biotechnol., 2012, 168(5), 1153-1162.
[http://dx.doi.org/10.1007/s12010-012-9848-8] [PMID: 22948604]
[17]
Mohamed, M.F.; Mohamed, M.S.; Fathi, M.M.; Shouman, S.A.; Abdelhamid, I.A. Chalcones incorporated pyrazole ring inhibit proliferation, cell cycle progression, angiogenesis and induce apoptosis of MCF7 cell line. Anticancer. Agents Med. Chem., 2014, 14(9), 1282-1292.
[http://dx.doi.org/10.2174/187152061409141010114547] [PMID: 25323033]
[18]
Sashidhara, K.V.; Kumar, A.; Kumar, M.; Sarkar, J.; Sinha, S. Synthesis and in vitro evaluation of novel coumarin-chalcone hybrids as potential anticancer agents. Bioorg. Med. Chem. Lett., 2010, 20(24), 7205-7211.
[http://dx.doi.org/10.1016/j.bmcl.2010.10.116] [PMID: 21071221]
[19]
Heidari, M.R.; Foroumadi, A.; Amirabadi, A.; Samzadeh-Kermani, A.; Azimzadeh, B.S.; Eskandarizadeh, A. Evaluation of anti-inflammatory and analgesic activity of a novel rigid 3, 4-dihydroxy chalcone in mice. Ann. N. Y. Acad. Sci., 2009, 1171(1), 399-406.
[http://dx.doi.org/10.1111/j.1749-6632.2009.04904.x] [PMID: 19723082]
[20]
Asiri, A.M.; Khan, S.A. Synthesis and anti-bacterial activities of a bis-chalcone derived from thiophene and its bis-cyclized products. Molecules, 2011, 16(1), 523-531.
[http://dx.doi.org/10.3390/molecules16010523] [PMID: 21228758]
[21]
Rueffer, M.; Amann, M.; Zenk, M.H. S-Adenosyl-L-methionine: Columbamine-O-methyl transferase, a compartmentalized enzyme in protoberberine biosynthesis. Plant Cell Rep., 1986, 5(3), 182-185.
[http://dx.doi.org/10.1007/BF00269113] [PMID: 24248127]
[22]
Huang, L.; Shi, A.; He, F.; Li, X. Synthesis, biological evaluation, and molecular modeling of berberine derivatives as potent acetylcholinesterase inhibitors. Bioorg. Med. Chem., 2010, 18(3), 1244-1251.
[http://dx.doi.org/10.1016/j.bmc.2009.12.035] [PMID: 20056426]
[23]
Galat, A. Synthesis of papaverine and some related compounds. J. Am. Chem. Soc., 1951, 73(8), 3654-3656.
[http://dx.doi.org/10.1021/ja01152a027]
[24]
Elwan, N.M.; Abdelhadi, H.A.; Abdallah, T.A.; Hassaneen, H.M. Synthesis of [1,2,4]triazolo[3,4-a]isoquinolines and pyrrolo[2,1-a]Isoquinolines using α-keto hydrazonoyl halides. Tetrahedron, 1996, 52(10), 3451-3456.
[http://dx.doi.org/10.1016/0040-4020(96)00024-5]
[25]
Barbosa-Filho, J.M.; Piuvezam, M.R.; Moura, M.D.; Silva, M.S.; Lima, K.V.B.; da-Cunha, E.V.L.; Fechine, I.M.; Takemura, O.S. Anti-inflammatory activity of alkaloids: A Twenty-century review. Rev. Bras. Farmacogn., 2006, 16(1), 109-139.
[http://dx.doi.org/10.1590/S0102-695X2006000100020]
[26]
Küpeli, E.; Koşar, M.; Yeşilada, E.; Hüsnü, K.; Başer, C. A comparative study on the anti-inflammatory, antinociceptive and antipyretic effects of isoquinoline alkaloids from the roots of Turkish Berberis species. Life Sci., 2002, 72(6), 645-657.
[http://dx.doi.org/10.1016/S0024-3205(02)02200-2] [PMID: 12467905]
[27]
Mukherjee, A.; Dutta, S.; Shanmugavel, M.; Mondhe, D.M.; Sharma, P.R.; Singh, S.K.; Saxena, A.K.; Sanyal, U. 6-Nitro-2-(3-hydroxypropyl)-1H-benz[de]isoquinoline-1,3-dione, a potent antitumor agent, induces cell cycle arrest and apoptosis. J. Exp. Clin. Cancer Res., 2010, 29(1), 175.
[http://dx.doi.org/10.1186/1756-9966-29-175] [PMID: 21194464]
[28]
Mohamed, M.F.; Hassaneen, H.M.; Abdelhamid, I.A. Cytotoxicity, molecular modeling, cell cycle arrest, and apoptotic induction induced by novel tetrahydro-[1,2,4]triazolo[3,4-a]isoquinoline chalcones. Eur. J. Med. Chem., 2018, 143(1), 532-541.
[http://dx.doi.org/10.1016/j.ejmech.2017.11.045] [PMID: 29207336]
[29]
Yang, X.; Yang, S.; Chai, H.; Yang, Z.; Lee, R.J.; Liao, W.; Teng, L. A novel isoquinoline derivative anticancer agent and its targeted delivery to tumor cells using transferrin-conjugated liposomes. PLoS One, 2015, 10(8)e0136649
[http://dx.doi.org/10.1371/journal.pone.0136649] [PMID: 26309138]
[30]
Jain, A.K.; Sharma, S.; Vaidya, A.; Ravichandran, V.; Agrawal, R.K. 1,3,4-thiadiazole and its derivatives: a review on recent progress in biological activities. Chem. Biol. Drug Des., 2013, 81(5), 557-576.
[http://dx.doi.org/10.1111/cbdd.12125] [PMID: 23452185]
[31]
Miller, K.D.; Siegel, R.L.; Lin, C.C.; Mariotto, A.B.; Kramer, J.L.; Rowland, J.H.; Stein, K.D.; Alteri, R.; Jemal, A. Cancer treatment and survivorship statistics, 2016. CA Cancer J. Clin., 2016, 66(4), 271-289.
[http://dx.doi.org/10.3322/caac.21349] [PMID: 27253694]
[32]
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2018. CA Cancer J. Clin., 2018, 68(1), 7-30.
[http://dx.doi.org/10.3322/caac.21442] [PMID: 29313949]
[33]
Lowe, S.W.; Lin, A.W. Apoptosis in cancer. Carcinogenesis, 2000, 21(3), 485-495.
[http://dx.doi.org/10.1093/carcin/21.3.485] [PMID: 10688869]
[34]
Ediriweera, M.K.; Tennekoon, K.H.; Samarakoon, S.R. In vitro assays and techniques utilized in anticancer drug discovery. J. Appl. Toxicol., 2019, 39(1), 38-71.
[35]
Ibrahim, N.S.; Mohamed, M.F.; Elwahy, A.H.M.; Abdelhamid, I.A. Biological activities and docking studies on novel bis 1,4-DHPS linked to arene core via ether or ester linkage. Lett. Drug Des. Discov., 2018, 15, 1036-1045.
[http://dx.doi.org/10.2174/1570180815666180105162323]
[36]
Abdella, A.M.; Mohamed, M.F.; Mohamed, A.F.; Elwahy, A.H.M.; Abdelhamid, I.A. Novel bis(dihydropyrano[3,2-c]chromenes): Synthesis, antiproliferative effect and molecular docking simulation. J. Heterocycl. Chem., 2018, 55(2), 498-507.
[http://dx.doi.org/10.1002/jhet.3072]
[37]
Khatab, T.K.; El-Bayouki, K.A.; Basyouni, W.M.; Sroor, F.M.A. Synthesis and structural characterization of new oxazole and thiazole derivatives as anti-cancer agents view project. Egypt. J. Chem., 2013, 56(4), 291-305.
[38]
Sroor, F.M.; Basyouni, W.M.; Tohamy, W.M.; Abdelhafez, T.H.; El-awady, M.K. Novel pyrrolo[2,3-d]pyrimidine derivatives: Design, synthesis, structure elucidation and in vitro anti-BVDV activity. Tetrahedron, 2019, 75130749
[http://dx.doi.org/10.1016/j.tet.2019.130749]
[39]
Farid, M. Synthesis and characterization of new biologically active pyrrolo[2,3-b]pyridine scaffolds. Org. Med. Chem. Int. J., 2019, 10
[http://dx.doi.org/10.19080/OMCIJ.2019.09.555752]
[40]
Sroor, F.M.; Khatab, T.K.; Basyouni, W.M.; El-Bayouki, K.A.M. Synthesis and molecular docking studies of some new thiosemicarbazone derivatives as HCV polymeraseinhibitors. Synth. Commun., 2019, 49(11), 1444-1456.
[http://dx.doi.org/10.1080/00397911.2019.1605443]
[41]
Sroor, F.M.; Abdelmoniem, A.M.; Abdelhamid, I.A. Facile synthesis, structural activity relationship, molecular modeling and in vitro biological evaluation of new urea derivatives with incorporated isoxazole and thiazole moieties as anticancer agents. Chem. Select, 2019, 4(34), 10113-10121.
[http://dx.doi.org/10.1002/slct.201901415]
[42]
Sroor, F.M.; Abbas, S.Y.; Basyouni, W.M.; El-Bayouki, K.A.M.; El-Mansy, M.F.; Aly, H.F.; Ali, S.A.; Arafa, A.F.; Haroun, A.A. Synthesis, structural characterization and in vivo anti-diabetic evaluation of some new sulfonylurea derivatives in normal and silicate coated nanoparticle forms as anti-hyperglycemic agents. Bioorg. Chem., 2019, 92103290
[http://dx.doi.org/10.1016/j.bioorg.2019.103290] [PMID: 31561109]
[43]
Mohamed, M.F.; Mohamed, M.S.; Fathi, M.M.; Shouman, S.A.; Abdelhamid, I.A. Chalcones incorporated pyrazole ring inhibit proliferation, cell cycle progression, angiogenesis and induce apoptosis of MCF7 cell line. Anticancer. Agents Med. Chem., 2014, 14(9), 1282-1292.
[http://dx.doi.org/10.2174/187152061409141010114547] [PMID: 25323033]
[44]
Abdella, A.M.; Moatasim, Y.; Ali, M.A.; Elwahy, A.H.M.; Abdelhamid, I.A. Synthesis and Anti-influenza virus activity of novel bis(4H-chromene-3-carbonitrile) derivatives. J. Heterocycl. Chem., 2017, 54(3), 1854-1862.
[http://dx.doi.org/10.1002/jhet.2776]
[45]
Ghozlan, S.A.S.; Mohamed, M.F.; Ahmed, A.G.; Shouman, S.A.; Attia, Y.M.; Abdelhamid, I.A. Cytotoxic and antimicrobial evaluations of novel apoptotic and anti-angiogenic spiro cyclic 2-oxindole derivatives of 2-amino-tetrahydroquinolin-5-one. Arch. Pharm. (Weinheim), 2015, 348(2), 113-124.
[http://dx.doi.org/10.1002/ardp.201400304] [PMID: 25664629]
[46]
Mohamed, M.F.; Abdelmoniem, A.M.; Elwahy, A.H.M.; Abdelhamid, I.A. DNA fragmentation, cell cycle arrest, and docking study of novel bis spiro-cyclic 2-oxindole of pyrimido[4,5-b]quinoline-4,6-dione derivatives against breast carcinoma. Curr. Cancer Drug Targets, 2018, 18(4), 372-381.
[http://dx.doi.org/10.2174/1568009617666170630143311] [PMID: 28669339]
[47]
Mohamed, M.F.; Ibrahim, N.S.; Elwahy, A.H.M.; Abdelhamid, I.A. Molecular studies on novel antitumor bis 1,4-dihydropyridine derivatives against lung carcinoma and their limited side effects on normal melanocytes. Anticancer. Agents Med. Chem., 2018, 18(15), 2156-2168.
[http://dx.doi.org/10.2174/1871520618666181019095007] [PMID: 30338746]
[48]
Salama, S.K.; Mohamed, M.F.; Darweesh, A.F.; Elwahy, A.H.M.; Abdelhamid, I.A. Molecular docking simulation and anticancer assessment on human breast carcinoma cell line using novel bis(1,4-dihydropyrano[2,3-c]pyrazole-5-carbonitrile) and bis(1,4-dihydropyrazolo[4′,3′:5,6]pyrano[2,3-b]pyridine-6-carbonitrile) derivatives. Bioorg. Chem., 2017, 71, 19-29.
[http://dx.doi.org/10.1016/j.bioorg.2017.01.009] [PMID: 28143658]
[49]
Mohamed, M.F.; Attia, Y.M.; Shouman, S.A.; Abdelhamid, I.A. Anticancer activities of new N-hetaryl-2-cyanoacetamide derivatives incorporating 4,5,6,7-tetrahydrobenzo[b]thiophene moiety. Anticancer. Agents Med. Chem., 2017, 17(8), 1084-1092.
[http://dx.doi.org/10.2174/1871520617666170110154110] [PMID: 28071583]
[50]
Mohamed, M.F.; Mohamed, A.F.; Abdelhamid, I.A. Antimicrobial, Sulphorhodamine (SRB) and antiviral evaluation of cyanoacrylamide derivatives. World J. Pharm. Sci., 2016, 4(1), 4-13.
[51]
El-Far, M.; Elmegeed, G.A.; Eskander, E.F.; Rady, H.M.; Tantawy, M.A. Novel modified steroid derivatives of androstanolone as chemotherapeutic anti-cancer agents. Eur. J. Med. Chem., 2009, 44(10), 3936-3946.
[http://dx.doi.org/10.1016/j.ejmech.2009.04.020] [PMID: 19447526]
[52]
Sebeka1, A.A.H.; Osman, A.M.A.; El Sayed, I.E.; El Bahanasawy, M.; Tantawy, M.A. Synthesis and antiproliferative activity of novel neocryptolepine hydrazides hybrids. J. Appl. Pharm. Sci., 2017, 7(10), 9-15.
[http://dx.doi.org/10.7324/JAPS.2017.71002]
[53]
Ranganathan, S.; Halagowder, D.; Sivasithambaram, N.D. Quercetin suppresses twist to induce apoptosis in MCF-7 breast cancer cells. PLoS One, 2015, 10(10)e0141370
[http://dx.doi.org/10.1371/journal.pone.0141370] [PMID: 26491966]
[54]
Tantawy, M.A.; Nafie, M.S.; Elmegeed, G.A.; Ali, I.A.I. Auspicious role of the steroidal heterocyclic derivatives as a platform for anti-cancer drugs. Bioorg. Chem., 2017, 73, 128-146.
[http://dx.doi.org/10.1016/j.bioorg.2017.06.006] [PMID: 28668650]
[55]
Ali, A.G.; Mohamed, M.F.; Abdelhamid, A.O.; Mohamed, M.S. A novel adamantane thiadiazole derivative induces mitochondria-mediated apoptosis in lung carcinoma cell line. Bioorg. Med. Chem., 2017, 25(1), 241-253.
[http://dx.doi.org/10.1016/j.bmc.2016.10.040] [PMID: 27847140]
[56]
Zhao, Y.; Xiang, S.; Dai, X.; Yang, K. A simplified diphenylamine colorimetric method for growth quantification. Appl. Microbiol. Biotechnol., 2013, 97(11), 5069-5077.
[http://dx.doi.org/10.1007/s00253-013-4893-y] [PMID: 23604560]
[57]
Preusse, M.; Tantawy, M.A.; Klawonn, F.; Schughart, K.; Pessler, F. Infection- and procedure-dependent effects on pulmonary gene expression in the early phase of influenza A virus infection in mice. BMC Microbiol., 2013, 13, 293.
[http://dx.doi.org/10.1186/1471-2180-13-293] [PMID: 24341411]
[58]
Petersen, H.; Mostafa, A.; Tantawy, M.A.; Iqbal, A.A.; Hoffmann, D.; Tallam, A.; Selvakumar, B.; Pessler, F.; Beer, M.; Rautenschlein, S.; Pleschka, S. NS segment of a 1918 Influenza A virus-descendent enhances replication of H1N1pdm09 and virus-induced cellular immune response in mammalian and avian systems. Front. Microbiol., 2018, 9, 526.
[http://dx.doi.org/10.3389/fmicb.2018.00526] [PMID: 29623073]
[59]
Hassaneen, H.M.; Hassaneen, H.M.E.; Mohammed, Y.S. Reactivity of 1-methylisoquinoline synthesis of pyrazolyl triazoloisoquinoline and thia-diazolyl isoquinoline derivatives. Nat. Sci., 2011, 03(08), 651-660.
[http://dx.doi.org/10.4236/ns.2011.38089]
[60]
Abdallah, T.A.; Abdelhadi, H.A.; Hassaneen, H.M. Reactivity of 1-methylisoquinoline. Synthesis of 2-(1-isoquinolinemethylidene)-1,3,4-thiadiazole derivatives. Phosphorus Sulfur Silicon Relat. Elem., 2002, 177(1), 59-66.
[http://dx.doi.org/10.1080/10426500210218]
[61]
Ranaivoson, F.M.; Gigant, B.; Berritt, S.; Joullié, M.; Knossow, M. IUCr Structural plasticity of tubulin assembly probed by vinca-domain ligands. Acta Crystallogr. D Biol. Crystallogr., 2012, 68(8), 927-934.
[http://dx.doi.org/10.1107/S0907444912017143] [PMID: 22868758]
[62]
Lewis, W.S.; Cody, V.; Galitsky, N.; Luft, J.R.; Pangborn, W.; Chunduru, S.K.; Spencer, H.T.; Appleman, J.R.; Blakley, R.L. Methotrexate-resistant variants of human dihydrofolate reductase with substitutions of leucine 22. Kinetics, crystallography, and potential as selectable markers. J. Biol. Chem., 1995, 270(10), 5057-5064.
[http://dx.doi.org/10.1074/jbc.270.10.5057] [PMID: 7890613]
[63]
Okamoto, K.; Ikemori-Kawada, M.; Jestel, A.; von König, K.; Funahashi, Y.; Matsushima, T.; Tsuruoka, A.; Inoue, A.; Matsui, J. Distinct binding mode of multikinase inhibitor lenvatinib revealed by biochemical characterization. ACS Med. Chem. Lett., 2014, 6(1), 89-94.
[http://dx.doi.org/10.1021/ml500394m] [PMID: 25589937]
[64]
Cossu, F.; Mastrangelo, E.; Milani, M.; Sorrentino, G.; Lecis, D.; Delia, D.; Manzoni, L.; Seneci, P.; Scolastico, C.; Bolognesi, M. Designing Smac-mimetics as antagonists of XIAP, cIAP1, and cIAP2. Biochem. Biophys. Res. Commun., 2009, 378(2), 162-167.
[http://dx.doi.org/10.1016/j.bbrc.2008.10.139] [PMID: 18992220]
[65]
Cui, J.J.; Tran-Dubé, M.; Shen, H.; Nambu, M.; Kung, P-P.; Pairish, M.; Jia, L.; Meng, J.; Funk, L.; Botrous, I.; McTigue, M.; Grodsky, N.; Ryan, K.; Padrique, E.; Alton, G.; Timofeevski, S.; Yamazaki, S.; Li, Q.; Zou, H.; Christensen, J.; Mroczkowski, B.; Bender, S.; Kania, R.S.; Edwards, M.P. Structure based drug design of crizotinib (PF-02341066), a potent and selective dual inhibitor of mesenchymal-epithelial transition factor (c-MET) kinase and anaplastic lymphoma kinase (ALK). J. Med. Chem., 2011, 54(18), 6342-6363.
[http://dx.doi.org/10.1021/jm2007613] [PMID: 21812414]
[66]
Stamos, J.; Sliwkowski, M.X.; Eigenbrot, C. Structure of the epidermal growth factor receptor kinase domain alone and in complex with a 4-anilinoquinazoline inhibitor. J. Biol. Chem., 2002, 277(48), 46265-46272.
[http://dx.doi.org/10.1074/jbc.M207135200] [PMID: 12196540]
[67]
Pedrini, F.S.; Chiaradia, L.D.; Licínio, M.A.; de Moraes, A.C.R.; Curta, J.C.; Costa, A.; Mascarello, A.; Creczinsky-Pasa, T.B.; Nunes, R.J.; Yunes, R.A.; Santos-Silva, M.C. Induction of apoptosis and cell cycle arrest in L-1210 murine lymphoblastic leukaemia cells by (2E)-3-(2-naphthyl)-1-(3′-methoxy-4′-hydroxy-phenyl)-2-propen-1-one. J. Pharm. Pharmacol., 2010, 62(9), 1128-1136.
[http://dx.doi.org/10.1111/j.2042-7158.2010.01141.x] [PMID: 20796191]
[68]
Rozmer, Z.; Berki, T.; Perjési, P. Different effects of two cyclic chalcone analogues on cell cycle of Jurkat T cells. Toxicol. In Vitro, 2006, 20, 1354-1362.https://doi.org/https://doi.org/10.1016/j.tiv.2006.05.006
[69]
Rao, Y.K.; Fang, S-H.; Tzeng, Y-M. Differential effects of synthesized 2′-oxygenated chalcone derivatives: modulation of human cell cycle phase distribution. Bioorg. Med. Chem., 2004, 12(10), 2679-2686.
[http://dx.doi.org/10.1016/j.bmc.2004.03.014] [PMID: 15110849]
[70]
Liu, X.; Go, M-L. Antiproliferative properties of piperidinylchalcones. Bioorg. Med. Chem., 2006, 14(1), 153-163.
[http://dx.doi.org/10.1016/j.bmc.2005.08.006] [PMID: 16185876]
[71]
Kousholt, A.N.; Menzel, T.; Sørensen, C.S.; Kousholt, A.N.; Menzel, T.; Sørensen, C.S. Pathways for genome integrity in G2 phase of the cell cycle. Biomolecules, 2012, 2(4), 579-607.
[http://dx.doi.org/10.3390/biom2040579] [PMID: 24970150]
[72]
Hochegger, H.; Takeda, S.; Hunt, T. Cyclin-dependent kinases and cell-cycle transitions: does one fit all? Nat. Rev. Mol. Cell Biol., 2008, 9(11), 910-916.
[http://dx.doi.org/10.1038/nrm2510] [PMID: 18813291]
[73]
Suryadinata, R.; Sadowski, M.; Sarcevic, B. Control of cell cycle progression by phosphorylation of cyclin-dependent kinase (CDK) substrates. Biosci. Rep., 2010, 30(4), 243-255.
[http://dx.doi.org/10.1042/BSR20090171] [PMID: 20337599]
[74]
Buommino, E.; Nicoletti, R.; Gaeta, G.M.; Orlando, M.; Ciavatta, M.L.; Baroni, A.; Tufano, M.A. 3-O-methylfunicone, a secondary metabolite produced by Penicillium pinophilum, induces growth arrest and apoptosis in HeLa cells. Cell Prolif., 2004, 37(6), 413-426.
[http://dx.doi.org/10.1111/j.1365-2184.2004.00323.x] [PMID: 15548174]
[75]
Gavet, O.; Pines, J. Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis. J. Cell Biol., 2010, 189(2), 247-259.
[http://dx.doi.org/10.1083/jcb.200909144] [PMID: 20404109]
[76]
Zhang, L.J.; Hao, Y.Z.; Hu, C.S.; Ye, Y.; Xie, Q.P.; Thorne, R.F.; Hersey, P.; Zhang, X.D. Inhibition of apoptosis facilitates necrosis induced by cisplatin in gastric cancer cells. Anticancer Drugs, 2008, 19(2), 159-166.
[http://dx.doi.org/10.1097/CAD.0b013e3282f30d05] [PMID: 18176112]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 20
ISSUE: 1
Year: 2020
Page: [70 - 83]
Pages: 14
DOI: 10.2174/1871520619666191024121116
Price: $65

Article Metrics

PDF: 35
HTML: 9
PRC: 1