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Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

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

Review Article

Anti-Cancer Stem Cells Potentiality of an Anti-Malarial Agent Quinacrine: An Old Wine in a New Bottle

Author(s): Biswajit Das and Chanakya N. Kundu*

Volume 21 , Issue 4 , 2021

Published on: 21 July, 2020

Page: [416 - 427] Pages: 12

DOI: 10.2174/1871520620666200721123046

Price: $65

Abstract

Quinacrine (QC) is a tricyclic compound and a derivative of 9-aminoacridine. It has been widely used to treat malaria and other parasitic diseases since the last century. Interestingly, studies have revealed that it also displays anti-cancer activities. Here, we have discussed the anti-cancer mechanism of QC along with its potentiality to specifically target cancer stem cells. The anti-cancer action of this drug includes DNA intercalation, inhibition of DNA repair mechanism, prevention of cellular growth, cell cycle arrest, inhibition of DNA and RNA polymerase activity, induction of autophagy, promotion of apoptosis, deregulation of cell signaling in cancer cells and cancer stem cells, inhibition of metastasis and angiogenesis. In addition, we have also emphasized on the synergistic effect of this drug with other potent chemotherapeutic agents and mentioned its different applications in anti-cancer therapy.

Keywords: Quinacrine, anti-cancer potentiality, cancer stem cells, metastasis, angiogenesis, cancer stem cell signaling.

Graphical Abstract
[1]
Ehsanian, R.; Van Waes, C.; Feller, S.M. Beyond DNA binding - a review of the potential mechanisms mediating quinacrine’s therapeutic activities in parasitic infections, inflammation, and cancers. Cell Commun. Signal., 2011, 9(1), 13.
[http://dx.doi.org/10.1186/1478-811X-9-13] [PMID: 21569639]
[2]
Yan, H.; Bian, A.; Gao, X.; Li, H.; Chen, Z.; Liu, X. Novel applications for an established antimalarial drug: Tumoricidal activity of quinacrine. Future Oncol., 2018, 14(15), 1511-1520.
[http://dx.doi.org/10.2217/fon-2017-0728] [PMID: 29380639]
[3]
Gurova, K.V.; Hill, J.E.; Guo, C.; Prokvolit, A.; Burdelya, L.G.; Samoylova, E.; Khodyakova, A.V.; Ganapathi, R.; Ganapathi, M.; Tararova, N.D.; Bosykh, D.; Lvovskiy, D.; Webb, T.R.; Stark, G.R.; Gudkov, A.V. Small molecules that reactivate p53 in renal cell carcinoma reveal a NF-kappaB-dependent mechanism of p53 suppression in tumors. Proc. Natl. Acad. Sci. USA, 2005, 102(48), 17448-17453.
[http://dx.doi.org/10.1073/pnas.0508888102] [PMID: 16287968]
[4]
de Souza, P.L.; Castillo, M.; Myers, C.E. Enhancement of paclitaxel activity against hormone-refractory prostate cancer cells in vitro and in vivo by quinacrine. Br. J. Cancer, 1997, 75(11), 1593-1600.
[http://dx.doi.org/10.1038/bjc.1997.272] [PMID: 9184173]
[5]
Illanes, J.; Dabancens, A.; Acuña, O.; Fuenzalida, M.; Guerrero, A.; Lopez, C.; Lemus, D. Effects of betamethasone, sulindac and quinacrine drugs on the inflammatory neoangiogenesis response induced by polyurethane sponge implanted in mouse. Biol. Res., 2002, 35(3-4), 339-345.
[http://dx.doi.org/10.4067/S0716-97602002000300008] [PMID: 12462986]
[6]
Zhu, S.; Chen, Z.; Wang, L.; Peng, D.; Belkhiri, A.; Lockhart, A.C.; El-Rifai, W. A combination of SAHA and quinacrine is effective in inducing cancer cell death in upper gastrointestinal cancers. Clin. Cancer Res., 2018, 24(8), 1905-1916.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-1716] [PMID: 29386219]
[7]
Siddharth, S.; Nayak, D.; Nayak, A.; Das, S.; Kundu, C.N. ABT-888 and quinacrine induced apoptosis in metastatic breast cancer stem cells by inhibiting base excision repair via adenomatous polyposis coli. DNA Repair (Amst.), 2016, 45, 44-55.
[http://dx.doi.org/10.1016/j.dnarep.2016.05.034] [PMID: 27334689]
[8]
Das, S.; Tripathi, N.; Siddharth, S.; Nayak, A.; Nayak, D.; Sethy, C.; Bharatam, P.V.; Kundu, C.N. Etoposide and doxorubicin enhance the sensitivity of triple negative breast cancers through modulation of TRAIL-DR5 axis. Apoptosis, 2017, 22(10), 1205-1224.
[http://dx.doi.org/10.1007/s10495-017-1400-4] [PMID: 28702823]
[9]
Abdulghani, J.; Gokare, P.; Gallant, J.N.; Dicker, D.; Whitcomb, T.; Cooper, T.; Liao, J.; Derr, J.; Liu, J.; Goldenberg, D.; Finnberg, N.K.; El-Deiry, W.S. Sorafenib and quinacrine target anti-apoptotic protein MCL1: A poor prognostic marker in Anaplastic Thyroid Cancer (ATC). Clin. Cancer Res., 2016, 22(24), 6192-6203.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-2792] [PMID: 27307592]
[10]
Sun, M.G.; Shi, J.F.; Li, X.Y.; Zhao, Y.; Ju, R.J.; Mu, L.M.; Yan, Y.; Li, X.T.; Zeng, F.; Lu, W.L. Targeting epirubicin plus quinacrine liposomes modified with DSPE-PEG2000-C (RGDfK) conjugate for eliminating invasive breast cancer. J. Biomed. Nanotechnol., 2015, 11(8), 1339-1353.
[http://dx.doi.org/10.1166/jbn.2015.2079] [PMID: 26295137]
[11]
Li, X.T.; Zhou, Z.Y.; Jiang, Y.; He, M.L.; Jia, L.Q.; Zhao, L.; Cheng, L.; Jia, T.Z. PEGylated VRB plus quinacrine cationic liposomes for treating non-small cell lung cancer. J. Drug Target., 2015, 23(3), 232-243.
[http://dx.doi.org/10.3109/1061186X.2014.979829] [PMID: 25417934]
[12]
Lobo, M.R.; Green, S.C.; Schabel, M.C.; Gillespie, G.Y.; Woltjer, R.L.; Pike, M.M. Quinacrine synergistically enhances the antivascular and antitumor efficacy of cediranib in intracranial mouse glioma. Neuro-oncol., 2013, 15(12), 1673-1683.
[http://dx.doi.org/10.1093/neuonc/not119] [PMID: 24092859]
[13]
Wang, Y.; Bi, Q.; Dong, L.; Li, X.; Ge, X.; Zhang, X.; Fu, J.; Wu, D.; Li, S. Quinacrine enhances cisplatin-induced cytotoxicity in four cancer cell lines. Chemotherapy, 2010, 56(2), 127-134.
[http://dx.doi.org/10.1159/000313525] [PMID: 20407239]
[14]
Gallant, J.N.; Allen, J.E.; Smith, C.D.; Dicker, D.T.; Wang, W.; Dolloff, N.G.; Navaraj, A.; El-Deiry, W.S. Quinacrine synergizes with 5-fluorouracil and other therapies in colorectal cancer. Cancer Biol. Ther., 2011, 12(3), 239-251.
[http://dx.doi.org/10.4161/cbt.12.3.17034] [PMID: 21725213]
[15]
Reyes, S.; Herrera, L.A.; Ostrosky, P.; Sotelo, J. Quinacrine enhances carmustine therapy of experimental rat glioma. Neurosurgery, 2001, 49(4), 969-973.
[PMID: 11564260]
[16]
Jani, T.S.; DeVecchio, J.; Mazumdar, T.; Agyeman, A.; Houghton, J.A. Inhibition of NF-kappaB signaling by quinacrine is cytotoxic to human colon carcinoma cell lines and is synergistic in combination with Tumor necrosis factor-Related Apoptosis-Inducing Ligand (TRAIL) or oxaliplatin. J. Biol. Chem., 2010, 285(25), 19162-19172.
[http://dx.doi.org/10.1074/jbc.M109.091645] [PMID: 20424169]
[17]
Liang, G.W.; Lu, W.L.; Wu, J.W.; Zhao, J.H.; Hong, H.Y.; Long, C.; Li, T.; Zhang, Y.T.; Zhang, H.; Wang, J.C.; Zhang, X.; Zhang, Q. Enhanced therapeutic effects on the multi-drug resistant human leukemia cells in vitro and xenograft in mice using the stealthy liposomal vincristine plus quinacrine. Fundam. Clin. Pharmacol., 2008, 22(4), 429-437.
[http://dx.doi.org/10.1111/j.1472-8206.2008.00613.x] [PMID: 18705753]
[18]
Preet, R.; Siddharth, S.; Satapathy, S.R.; Das, S.; Nayak, A.; Das, D.; Wyatt, M.D.; Kundu, C.N. Chk1 inhibitor synergizes quinacrine mediated apoptosis in breast cancer cells by compromising the base excision repair cascade. Biochem. Pharmacol., 2016, 105, 23-33.
[http://dx.doi.org/10.1016/j.bcp.2016.01.017] [PMID: 26850987]
[19]
Zhang, L.; Yao, H.J.; Yu, Y.; Zhang, Y.; Li, R.J.; Ju, R.J.; Wang, X.X.; Sun, M.G.; Shi, J.F.; Lu, W.L. Mitochondrial targeting liposomes incorporating daunorubicin and quinacrine for treatment of relapsed breast cancer arising from cancer stem cells. Biomaterials, 2012, 33(2), 565-582.
[http://dx.doi.org/10.1016/j.biomaterials.2011.09.055] [PMID: 21983136]
[20]
Wang, W.; Gallant, J.N.; Katz, S.I.; Dolloff, N.G.; Smith, C.D.; Abdulghani, J.; Allen, J.E.; Dicker, D.T.; Hong, B.; Navaraj, A.; El-Deiry, W.S. Quinacrine sensitizes hepatocellular carcinoma cells to TRAIL and chemotherapeutic agents. Cancer Biol. Ther., 2011, 12(3), 229-238.
[http://dx.doi.org/10.4161/cbt.12.3.17033] [PMID: 21725212]
[21]
Matteoni, S.; Abbruzzese, C.; Matarrese, P.; De Luca, G.; Mileo, A.M.; Miccadei, S.; Schenone, S.; Musumeci, F.; Haas, T.L.; Sette, G.; Carapella, C.M.; Amato, R.; Perrotti, N.; Signore, M.; Paggi, M.G. The kinase inhibitor SI113 induces autophagy and synergizes with quinacrine in hindering the growth of human glioblastoma multiforme cells. J. Exp. Clin. Cancer Res., 2019, 38(1), 202.
[http://dx.doi.org/10.1186/s13046-019-1212-1] [PMID: 31101126]
[22]
Eriksson, A.; Chantzi, E.; Fryknäs, M.; Gullbo, J.; Nygren, P.; Gustafsson, M.; Höglund, M.; Larsson, R. Towards repositioning of quinacrine for treatment of acute myeloid leukemia - Promising synergies and in vivo effects. Leuk. Res., 2017, 63, 41-46.
[http://dx.doi.org/10.1016/j.leukres.2017.10.012] [PMID: 29100024]
[23]
Sotelo, J.; Guevara, P.; Pineda, B.; Diaz, C. Interstitial quinacrine activates a distinctive immune response effective for tumor immunotherapy. Surgery, 2004, 136(3), 700-707.
[http://dx.doi.org/10.1016/j.surg.2004.01.008] [PMID: 15349121]
[24]
Robinson, N.J.; Taylor, D.J.; Schiemann, W.P. Stem cells, immortality, and the evolution of metastatic properties in breast cancer: Telomere maintenance mechanisms and metastatic evolution. J. Cancer Metastasis Treat., 2019, 5, 39.
[http://dx.doi.org/10.20517/2394-4722.2019.15] [PMID: 31440584]
[25]
Satapathy, S.R.; Siddharth, S.; Das, D.; Nayak, A.; Kundu, C.N. Enhancement of cytotoxicity and inhibition of angiogenesis in oral cancer stem cells by a hybrid nanoparticle of bioactive quinacrine and silver: Implication of base excision repair cascade. Mol. Pharm., 2015, 12(11), 4011-4025.
[http://dx.doi.org/10.1021/acs.molpharmaceut.5b00461] [PMID: 26448277]
[26]
Satapathy, S.R.; Nayak, A.; Siddharth, S.; Das, S.; Nayak, D.; Kundu, C.N. Metallic gold and bioactive quinacrine hybrid nanoparticles inhibit oral cancer stem cell and angiogenesis by deregulating inflammatory cytokines in p53 dependent manner. Nanomedicine (Lond.), 2018, 14(3), 883-896.
[http://dx.doi.org/10.1016/j.nano.2018.01.007] [PMID: 29366881]
[27]
Nayak, A.; Siddharth, S.; Das, S.; Nayak, D.; Sethy, C.; Kundu, C.N. Nanoquinacrine caused apoptosis in oral cancer stem cells by disrupting the interaction between GLI1 and β catenin through activation of GSK3β. Toxicol. Appl. Pharmacol., 2017, 330, 53-64.
[http://dx.doi.org/10.1016/j.taap.2017.07.008] [PMID: 28720477]
[28]
Hembram, K.C.; Chatterjee, S.; Sethy, C.; Nayak, D.; Pradhan, R.; Molla, S.; Bindhani, B.K.; Kundu, C.N. Comparative and mechanistic study on the anticancer activity of quinacrine-based silver and gold hybrid nanoparticles in head and neck cancer. Mol. Pharm., 2019, 16(7), 3011-3023.
[http://dx.doi.org/10.1021/acs.molpharmaceut.9b00242] [PMID: 31145852]
[29]
Nayak, A.; Das, S.; Nayak, D.; Sethy, C.; Narayan, S.; Kundu, C.N. Nanoquinacrine sensitizes 5-FU-resistant cervical cancer stem-like cells by down-regulating Nectin-4 via ADAM-17 mediated NOTCH deregulation. Cell Oncol. (Dordr.), 2019, 42(2), 157-171.
[http://dx.doi.org/10.1007/s13402-018-0417-1] [PMID: 30603978]
[30]
Guo, C.; Gasparian, A.V.; Zhuang, Z.; Bosykh, D.A.; Komar, A.A.; Gudkov, A.V.; Gurova, K.V. 9-Aminoacridine-based anticancer drugs target the PI3K/AKT/mTOR, NF-kappaB and p53 pathways. Oncogene, 2009, 28(8), 1151-1161.
[http://dx.doi.org/10.1038/onc.2008.460] [PMID: 19137016]
[31]
Zhong, H.; May, M.J.; Jimi, E.; Ghosh, S. The phosphorylation status of nuclear NF-κB determines its association with CBP/p300 or HDAC-1. Mol. Cell, 2002, 9(3), 625-636.
[http://dx.doi.org/10.1016/S1097-2765(02)00477-X] [PMID: 11931769]
[32]
Hayden, M.S.; West, A.P.; Ghosh, S. NF-kappaB and the immune response. Oncogene, 2006, 25(51), 6758-6780.
[http://dx.doi.org/10.1038/sj.onc.1209943] [PMID: 17072327]
[33]
Magnaghi-Jaulin, L.; Groisman, R.; Naguibneva, I.; Robin, P.; Lorain, S.; Le Villain, J.P.; Troalen, F.; Trouche, D.; Harel-Bellan, A. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature, 1998, 391(6667), 601-605.
[http://dx.doi.org/10.1038/35410] [PMID: 9468140]
[34]
Dermawan, J.K.; Gurova, K.; Pink, J.; Dowlati, A.; De, S.; Narla, G.; Sharma, N.; Stark, G.R. Quinacrine overcomes resistance to erlotinib by inhibiting FACT, NF-κB, and cell-cycle progression in non-small cell lung cancer. Mol. Cancer Ther., 2014, 13(9), 2203-2214.
[http://dx.doi.org/10.1158/1535-7163.MCT-14-0013] [PMID: 25028470]
[35]
Aslanoglu, M.; Ayne, G. Voltammetric studies of the interaction of quinacrine with DNA. Anal. Bioanal. Chem., 2004, 380(4), 658-663.
[http://dx.doi.org/10.1007/s00216-004-2797-5] [PMID: 15316709]
[36]
Gurova, K. New hopes from old drugs: Revisiting DNA-binding small molecules as anticancer agents. Future Oncol., 2009, 5(10), 1685-1704.
[http://dx.doi.org/10.2217/fon.09.127] [PMID: 20001804]
[37]
Demeunynck, M.; Charmantray, F.; Martelli, A. Interest of acridine derivatives in the anticancer chemotherapy. Curr. Pharm. Des., 2001, 7(17), 1703-1724.
[http://dx.doi.org/10.2174/1381612013397131] [PMID: 11562307]
[38]
Finlay, G.J.; Wilson, W.R.; Baguley, B.C. Chemoprotection by 9-aminoacridine derivatives against the cytotoxicity of topoisomerase II-directed drugs. Eur. J. Cancer Clin. Oncol., 1989, 25(12), 1695-1701.
[http://dx.doi.org/10.1016/0277-5379(89)90337-4] [PMID: 2561099]
[39]
Preet, R.; Mohapatra, P.; Mohanty, S.; Sahu, S.K.; Choudhuri, T.; Wyatt, M.D.; Kundu, C.N. Quinacrine has anticancer activity in breast cancer cells through inhibition of topoisomerase activity. Int. J. Cancer, 2012, 130(7), 1660-1670.
[http://dx.doi.org/10.1002/ijc.26158] [PMID: 21544805]
[40]
Eriksson, A.; Österroos, A.; Hassan, S.; Gullbo, J.; Rickardson, L.; Jarvius, M.; Nygren, P.; Fryknäs, M.; Höglund, M.; Larsson, R. Drug screen in patient cells suggests quinacrine to be repositioned for treatment of acute myeloid leukemia. Blood Cancer J., 2015, 5(4)e307
[http://dx.doi.org/10.1038/bcj.2015.31]] [PMID: 25885427]
[41]
Wu, X.; Wang, Y.; Wang, H.; Wang, Q.; Wang, L.; Miao, J.; Cui, F.; Wang, J. Quinacrine inhibits cell growth and induces apoptosis in human gastric cancer cell line SGC-7901 Curr. Ther. Res. Clin. Exp, 2012, 73(1-2), 52-64.
[42]
Gasparian, A.V.; Burkhart, C.A.; Purmal, A.A.; Brodsky, L.; Pal, M.; Saranadasa, M.; Bosykh, D.A.; Commane, M.; Guryanova, O.A.; Pal, S.; Safina, A.; Sviridov, S.; Koman, I.E.; Veith, J.; Komar, A.A.; Gudkov, A.V.; Gurova, K.V. Curaxins: Anticancer compounds that simultaneously suppress NF-κB and activate p53 by targeting FACT. Sci. Transl. Med., 2011, 3(95)95ra74
[http://dx.doi.org/10.1126/scitranslmed.3002530] [PMID: 21832239]
[43]
Belotserkovskaya, R.; Oh, S.; Bondarenko, V.A.; Orphanides, G.; Studitsky, V.M.; Reinberg, D. FACT facilitates transcription-dependent nucleosome alteration. Science, 2003, 301(5636), 1090-1093.
[http://dx.doi.org/10.1126/science.1085703] [PMID: 12934006]
[44]
Garcia, H.; Miecznikowski, J.C.; Safina, A.; Commane, M.; Ruusulehto, A.; Kilpinen, S.; Leach, R.W.; Attwood, K.; Li, Y.; Degan, S.; Omilian, A.R.; Guryanova, O.; Papantonopoulou, O.; Wang, J.; Buck, M.; Liu, S.; Morrison, C.; Gurova, K.V. Facilitates chromatin transcription complex is an “accelerator” of tumor transformation and potential marker and target of aggressive cancers. Cell Rep., 2013, 4(1), 159-173.
[http://dx.doi.org/10.1016/j.celrep.2013.06.013] [PMID: 23831030]
[45]
Oien, D.B.; Pathoulas, C.L.; Ray, U.; Thirusangu, P.; Kalogera, E.; Shridhar, V. Repurposing quinacrine for treatment-refractory cancer. Semin. Cancer Biol 2019 [In Press]. ,
[http://dx.doi.org/10.1016/j.semcancer.2019.09.021]
[46]
Jung, D.; Khurana, A.; Roy, D.; Kalogera, E.; Bakkum-Gamez, J.; Chien, J.; Shridhar, V. Quinacrine upregulates p21/p27 independent of p53 through autophagy-mediated downregulation of p62-Skp2 axis in ovarian cancer. Sci. Rep., 2018, 8(1), 2487.
[http://dx.doi.org/10.1038/s41598-018-20531-w] [PMID: 29410485]
[47]
Sherr, C.J.; Roberts, J.M. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev., 1999, 13(12), 1501-1512.
[http://dx.doi.org/10.1101/gad.13.12.1501] [PMID: 10385618]
[48]
Yang, S.; Sheng, L.; Xu, K.; Wang, Y.; Zhu, H.; Zhang, P.; Mu, Q.; Ouyang, G. Anticancer effect of quinacrine on diffuse large B cell lymphoma via inhibition of MSI2 NUMB signaling pathway. Mol. Med. Rep., 2018, 17(1), 522-530.
[49]
Sabzichi, M.; Ramezani, M.; Mohammadian, J.; Ghorbani, M.; Mardomi, A.; Najafipour, F.; Mehdizadeh, A. The synergistic impact of quinacrine on cell cycle and anti-invasiveness behaviors of doxorubicin in MDA-MB-231 breast cancer cells Process Biochem., 2019, 81(1), 175-181.
[http://dx.doi.org/10.1016/j.procbio.2019.03.007]
[50]
Kawade, V.S.; Satpute, P.S.; Dhulap, S.A.; Gurjar, S. Therapeutic potential of PI3K/Akt/mTOR signalling pathway: Effective combination therapy for cancer. Indian J. Pharm. Sci, 2018, 80(4), 702-708.
[http://dx.doi.org/10.4172/pharmaceutical-sciences.1000410]
[51]
Jackson, J.G.; Pant, V.; Li, Q.; Chang, L.L.; Quintás-Cardama, A.; Garza, D.; Tavana, O.; Yang, P.; Manshouri, T.; Li, Y.; El-Naggar, A.K.; Lozano, G. p53-mediated senescence impairs the apoptotic response to chemotherapy and clinical outcome in breast cancer. Cancer Cell, 2012, 21(6), 793-806.
[http://dx.doi.org/10.1016/j.ccr.2012.04.027] [PMID: 22698404]
[52]
Park, S.; Oh, A.Y.; Cho, J.H.; Yoon, M.H.; Woo, T.G.; Kang, S.M.; Lee, H.Y.; Jung, Y.J.; Park, B.J. Therapeutic effect of quinacrine, an antiprotozoan drug, by selective suppression of p-CHK1/2 in p53-negative malignant cancers. Mol. Cancer Res., 2018, 16(6), 935-946.
[http://dx.doi.org/10.1158/1541-7786.MCR-17-0511] [PMID: 29545477]
[53]
Choi, A.M.; Ryter, S.W.; Levine, B. Autophagy in human health and disease. N. Engl. J. Med., 2013, 368(7), 651-662.
[http://dx.doi.org/10.1056/NEJMra1205406] [PMID: 23406030]
[54]
Nazio, F.; Bordi, M.; Cianfanelli, V.; Locatelli, F.; Cecconi, F. Autophagy and cancer stem cells: Molecular mechanisms and therapeutic applications. Cell Death Differ., 2019, 26(4), 690-702.
[http://dx.doi.org/10.1038/s41418-019-0292-y] [PMID: 30728463]
[55]
Wirawan, E.; Vanden Berghe, T.; Lippens, S.; Agostinis, P.; Vandenabeele, P. Autophagy: For better or for worse. Cell Res , 2012, 22(1), 43-61.
[http://dx.doi.org/10.1038/cr.2011.152] [PMID: 21912435]
[56]
Kuo, P.L.; Hsu, Y.L.; Cho, C.Y. Plumbagin induces G2-M arrest and autophagy by inhibiting the AKT/mammalian target of rapamycin pathway in breast cancer cells. Mol. Cancer Ther., 2006, 5(12), 3209-3221.
[http://dx.doi.org/10.1158/1535-7163.MCT-06-0478] [PMID: 17172425]
[57]
Turcotte, S.; Chan, D.A.; Sutphin, P.D.; Hay, M.P.; Denny, W.A.; Giaccia, A.J. A molecule targeting VHL-deficient renal cell carcinoma that induces autophagy. Cancer Cell, 2008, 14(1), 90-102.
[http://dx.doi.org/10.1016/j.ccr.2008.06.004] [PMID: 18598947]
[58]
Auparakkitanon, S.; Noonpakdee, W.; Ralph, R.K.; Denny, W.A.; Wilairat, P. Antimalarial 9-anilinoacridine compounds directed at hematin. Antimicrob. Agents Chemother., 2003, 47(12), 3708-3712.
[http://dx.doi.org/10.1128/AAC.47.12.3708-3712.2003] [PMID: 14638470]
[59]
Mohapatra, P.; Preet, R.; Das, D.; Satapathy, S.R.; Choudhuri, T.; Wyatt, M.D.; Kundu, C.N. Quinacrine-mediated autophagy and apoptosis in colon cancer cells is through a p53- and p21-dependent mechanism. Oncol. Res., 2012, 20(2-3), 81-91.
[http://dx.doi.org/10.3727/096504012X13473664562628] [PMID: 23193914]
[60]
Wang, W.; Ho, W.C.; Dicker, D.T.; MacKinnon, C.; Winkler, J.D.; Marmorstein, R.; El-Deiry, W.S. Acridine derivatives activate p53 and induce tumor cell death through Bax. Cancer Biol. Ther., 2005, 4(8), 893-898.
[http://dx.doi.org/10.4161/cbt.4.8.2134] [PMID: 16177561]
[61]
Changchien, J.J.; Chen, Y.J.; Huang, C.H.; Cheng, T.L.; Lin, S.R.; Chang, L.S. Quinacrine induces apoptosis in human leukemia K562 cells via p38 MAPK-elicited BCL2 down-regulation and suppression of ERK/c-Jun-mediated BCL2L1 expression. Toxicol. Appl. Pharmacol., 2015, 284(1), 33-41.
[http://dx.doi.org/10.1016/j.taap.2015.02.005] [PMID: 25684043]
[62]
Huang, C.H.; Lee, Y.C.; Chen, Y.J.; Wang, L.J.; Shi, Y.J.; Chang, L.S. Quinacrine induces the apoptosis of human leukemia U937 cells through FOXP3/miR-183/β-TrCP/SP1 axis-mediated BAX upregulation. Toxicol. Appl. Pharmacol., 2017, 334, 35-46.
[http://dx.doi.org/10.1016/j.taap.2017.08.019] [PMID: 28867437]
[63]
Zhang, P.; Li, N.; Kiang, K.M.; Zhu, Z.; Leung, G.W.; Cheng, S.Y.; Leung, G.K. Quinacrine enhances temozolomide cytotoxicity in temozolomide-sensitive and-resistant glioblastoma cells.Glioma, 2018, 1(5), 105.
[http://dx.doi.org/10.4103/glioma.glioma_37_18]
[64]
Vitale, I.; Manic, G.; De Maria, R.; Kroemer, G.; Galluzzi, L. DNA damage in stem cells. Mol. Cell, 2017, 66(3), 306-319.
[http://dx.doi.org/10.1016/j.molcel.2017.04.006] [PMID: 28475867]
[65]
Pons-Tostivint, E.; Thibault, B.; Guillermet-Guibert, J. Targeting PI3K signaling in combination cancer therapy. Trends Cancer, 2017, 3(6), 454-469.
[http://dx.doi.org/10.1016/j.trecan.2017.04.002] [PMID: 28718419]
[66]
Das, S.; Nayak, A.; Siddharth, S.; Nayak, D.; Narayan, S.; Kundu, C.N. TRAIL enhances quinacrine-mediated apoptosis in breast cancer cells through induction of autophagy via modulation of p21 and DR5 interactions. Cell Oncol. (Dordr.), 2017, 40(6), 593-607.
[http://dx.doi.org/10.1007/s13402-017-0347-3] [PMID: 28936683]
[67]
Powers, M.V.; Clarke, P.A.; Workman, P. Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell, 2008, 14(3), 250-262.
[http://dx.doi.org/10.1016/j.ccr.2008.08.002] [PMID: 18772114]
[68]
Neznanov, N.; Gorbachev, A.V.; Neznanova, L.; Komarov, A.P.; Gurova, K.V.; Gasparian, A.V.; Banerjee, A.K.; Almasan, A.; Fairchild, R.L.; Gudkov, A.V. Anti-malaria drug blocks proteotoxic stress response: Anti-cancer implications. Cell Cycle, 2009, 8(23), 3960-3970.
[http://dx.doi.org/10.4161/cc.8.23.10179] [PMID: 19901558]
[69]
Preet, R.; Mohapatra, P.; Das, D.; Satapathy, S.R.; Choudhuri, T.; Wyatt, M.D.; Kundu, C.N. Lycopene synergistically enhances quinacrine action to inhibit Wnt-TCF signaling in breast cancer cells through APC. Carcinogenesis, 2013, 34(2), 277-286.
[http://dx.doi.org/10.1093/carcin/bgs351] [PMID: 23129580]
[70]
Nayak, D.; Tripathi, N.; Kathuria, D.; Siddharth, S.; Nayak, A.; Bharatam, P.V.; Kundu, C. Quinacrine and curcumin synergistically increased the breast cancer stem cells death by inhibiting ABCG2 and modulating DNA damage repair pathway. Int. J. Biochem. Cell Biol., 2020, 119105682
[http://dx.doi.org/10.1016/j.biocel.2019.105682] [PMID: 31877386]
[71]
Insan, M.B.; Jaitak, V. New approaches to target cancer stem cells: Current scenario. Mini Rev. Med. Chem., 2014, 14(1), 20-34.
[http://dx.doi.org/10.2174/13895575113136660107] [PMID: 24195662]
[72]
de Sousa e Melo. F.; Kurtova, A.V.; Harnoss, J.M.; Kljavin, N.; Hoeck, J.D.; Hung, J.; Anderson, J.E.; Storm, E.E.; Modrusan, Z.; Koeppen, H.; Dijkgraaf, G.J.; Piskol, R.; de Sauvage, F.J. A distinct role for Lgr5+ stem cells in primary and metastatic colon cancer. Nature, 2017, 543(7647), 676-680.
[http://dx.doi.org/10.1038/nature21713] [PMID: 28358093]
[73]
Krishnapriya, S.; Sidhanth, C.; Manasa, P.; Sneha, S.; Bindhya, S.; Nagare, R.P.; Ramachandran, B.; Vishwanathan, P.; Murhekar, K.; Shirley, S.; Ganesan, T.S. Cancer stem cells contribute to angiogenesis and lymphangiogenesis in serous adenocarcinoma of the ovary. Angiogenesis, 2019, 22(3), 441-455.
[http://dx.doi.org/10.1007/s10456-019-09669-x] [PMID: 31161471]
[74]
Roebuck, K.A.; Finnegan, A. Regulation of intercellular adhesion molecule-1 (CD54) gene expression. J. Leukoc. Biol.,, 1999, 66(6), 876-888.
[http://dx.doi.org/10.1002/jlb.66.6.876] [PMID: 10614768]
[75]
Ramos, T.N.; Bullard, D.C.; Barnum, S.R. ICAM-1: Isoforms and phenotypes. J. Immunol., 2014, 192(10), 4469-4474.
[http://dx.doi.org/10.4049/jimmunol.1400135] [PMID: 24795464]
[76]
Wai Wong, C.; Dye, D.E.; Coombe, D.R. The role of immunoglobulin superfamily cell adhesion molecules in cancer metastasis. Int. J. Cell Biol., 2012, 2012340296
[http://dx.doi.org/10.1155/2012/340296] [PMID: 22272201]
[77]
Harada, M.; Morimoto, K.; Kondo, T.; Hiramatsu, R.; Okina, Y.; Muko, R.; Matsuda, I.; Kataoka, T. Quinacrine inhibits ICAM-1 transcription by blocking DNA binding of the NF-κB subunit p65 and sensitizes human lung adenocarcinoma A549 cells to TNF-α and the Fas ligand. Int. J. Mol. Sci., 2017, 18(12)E2603
[http://dx.doi.org/10.3390/ijms18122603] [PMID: 29207489]
[78]
Kirschmann, D.A.; Seftor, E.A.; Hardy, K.M.; Seftor, R.E.; Hendrix, M.J. Molecular pathways: Vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications. Clin. Cancer Res., 2012, 18(10), 2726-2732.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-3237] [PMID: 22474319]
[79]
Carmeliet, P.; Jain, R.K. Molecular mechanisms and clinical applications of angiogenesis. Nature, 2011, 473(7347), 298-307.
[http://dx.doi.org/10.1038/nature10144] [PMID: 21593862]
[80]
Rajabi, M.; Mousa, S.A. The role of angiogenesis in cancer treatment. Biomedicines, 2017, 5(2), 34.
[http://dx.doi.org/10.3390/biomedicines5020034] [PMID: 28635679]
[81]
Popanda, O.; Thielmann, H.W. The function of DNA topoisomerases in UV-induced DNA excision repair: Studies with specific inhibitors in permeabilized human fibroblasts. Carcinogenesis, 1992, 13(12), 2321-2328.
[http://dx.doi.org/10.1093/carcin/13.12.2321] [PMID: 1335377]
[82]
Thielmann, H.W.; Popanda, O.; Gersbach, H.; Gilberg, F. Various inhibitors of DNA topoisomerases diminish repair-specific DNA incision in UV-irradiated human fibroblasts. Carcinogenesis, 1993, 14(11), 2341-2351.
[http://dx.doi.org/10.1093/carcin/14.11.2341] [PMID: 8242865]
[83]
Davar, D.; Beumer, J.H.; Hamieh, L.; Tawbi, H. Role of PARP inhibitors in cancer biology and therapy. Curr. Med. Chem., 2012, 19(23), 3907-3921.
[http://dx.doi.org/10.2174/092986712802002464] [PMID: 22788767]
[84]
Ko, H.L.; Ren, E.C. Functional aspects of PARP1 in DNA repair and transcription. Biomolecules, 2012, 2(4), 524-548.
[http://dx.doi.org/10.3390/biom2040524] [PMID: 24970148]
[85]
Nayak, A.; Satapathy, S.R.; Das, D.; Siddharth, S.; Tripathi, N.; Bharatam, P.V.; Kundu, C. Nanoquinacrine induced apoptosis in cervical cancer stem cells through the inhibition of hedgehog-GLI1 cascade: Role of GLI-1. Sci. Rep., 2016, 6, 20600.
[http://dx.doi.org/10.1038/srep20600] [PMID: 26846872]
[86]
Barker, N.; Clevers, H. Mining the Wnt pathway for cancer therapeutics. Nat. Rev. Drug Discov., 2006, 5(12), 997-1014.
[http://dx.doi.org/10.1038/nrd2154] [PMID: 17139285]
[87]
Sethy, C.; Goutam, K.; Nayak, D.; Pradhan, R.; Molla, S.; Chatterjee, S.; Rout, N.; Wyatt, M.D.; Narayan, S.; Kundu, C.N. Clinical significance of a pvrl 4 encoded gene Nectin-4 in metastasis and angiogenesis for tumor relapse. J. Cancer Res. Clin. Oncol., 2020, 146(1), 245-259.
[http://dx.doi.org/10.1007/s00432-019-03055-2] [PMID: 31617074]

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