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Anti-Cancer Agents in Medicinal Chemistry

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

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Research Article

Proteomic Level Changes on Treatment in MCF-7/DDP Breast Cancer Drug- Resistant Cells

Author(s): Gongshen Jin*, Kangwei Wang, Yonghong Liu, Xianhu Liu, Xiaojing Zhang and Hao Zhang

Volume 20, Issue 6, 2020

Page: [687 - 699] Pages: 13

DOI: 10.2174/1871520620666200213102849

open access plus

Abstract

Background: LCL161, a SMAC’S small molecule mimetic, can bind to a variety of IAPs and activate Caspases. We found that on its own, LCL161induces apoptosis of drug-resistant breast cancer cells by binding to a variety of IAPs and activating Caspases. However, when LCL161 is used in combination with Caspase Inhibitors (CI), its capacity to induce apoptosis of breast cancer cells is enhanced.

Objective: To carry out proteomic and bioinformatics analysis of LCL161 in combination with CI. We aim to identify the key proteins and mechanisms of breast cancer drug-resistant apoptosis, thereby aiding in the breast cancer drug resistance treatment and identification of drug targeting markers.

Methods: Cell culture experiments were carried out to explore the effect of LCL161 combined with CI on the proliferation of breast cancer drug-resistant cells. Proteomic analysis was carried out to determine the protein expression differences between breast cancer drug-resistant cells and LCL161 combined with CI treated cells. Bioinformatics analysis was carried out to determine its mechanism of action. Validation of proteomics results was done using Parallel Reaction Monitoring (PRM).

Results: Cell culture experiments showed that LCL161 in combination with CI can significantly promote the apoptosis of breast cancer drug-resistant cells. Up-regulation of 92 proteins and down-regulation of 114 proteins protein were noted, of which 4 were selected for further validation.

Conclusion: Our results show that LCL161 combined with CI can promote the apoptosis of drug-resistant breast cancer cells by down-regulation of RRM2, CDK4, and ITGB1 expression through Cancer pathways, p53 or PI3K-AKT signaling pathway. In addition, the expression of CDK4, RRM2, and CDC20 can be down-regulated by the nuclear receptor pathway to affect DNA transcription and replication, thereby promoting apoptosis of breast cancer drug-resistant cells.

Keywords: Breast cancer, proteomics, smac mimetics, Caspase Inhibitors (CI), p53, PI3k-AKT.

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[1]
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]
[2]
Rapoport, B.L.; Demetriou, G.S.; Moodley, S.D.; Benn, C.A. When and how do I use neoadjuvant chemotherapy for breast cancer? Curr. Treat. Options Oncol., 2014, 15(1), 86-98.
[http://dx.doi.org/10.1007/s11864-013-0266-0] [PMID: 24306808]
[3]
Tang, Y.; Wang, Y.; Kiani, M.F.; Wang, B. Classification, treatment strategy, and associated drug resistance in breast cancer. Clin. Breast Cancer, 2016, 16(5), 335-343.
[http://dx.doi.org/10.1016/j.clbc.2016.05.012] [PMID: 27268750]
[4]
Jeselsohn, R.; Brown, M. How drug resistance takes shape. J. eLife., 2016, 5(2016-03-14), 5-.
[5]
Tamm, I.; Wang, Y.; Sausville, E.; Scudiero, D.A.; Vigna, N.; Oltersdorf, T.; Reed, J.C. IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res., 1998, 58(23), 5315-5320.
[PMID: 9850056]
[6]
Salvesen, G.S.; Duckett, C.S. IAP proteins: blocking the road to death’s door. Nat. Rev. Mol. Cell Biol., 2002, 3(6), 401-410.
[http://dx.doi.org/10.1038/nrm830] [PMID: 12042762]
[7]
Vasilikos, L.; Spilgies, L.M.; Knop, J.; Wong, W.W. Regulating the balance between necroptosis, apoptosis and inflammation by inhibitors of apoptosis proteins. Immunol. Cell Biol., 2017, 95(2), 160-165.
[http://dx.doi.org/10.1038/icb.2016.118] [PMID: 27904150]
[8]
Lee, E.F.; Harris, T.J.; Tran, S.; Evangelista, M.; Arulananda, S.; John, T.; Ramnac, C.; Hobbs, C.; Zhu, H.; Gunasingh, G.; Segal, D.; Behren, A.; Cebon, J.; Dobrovic, A.; Mariadason, J.M.; Strasser, A.; Rohrbeck, L.; Haass, N.K.; Herold, M.J.; Fairlie, W.D. BCL-XL and MCL-1 are the key BCL-2 family proteins in melanoma cell survival. Cell Death Dis., 2019, 10(5), 342.
[http://dx.doi.org/10.1038/s41419-019-1568-3] [PMID: 31019203]
[9]
Mescolini, G.; Lupini, C.; Felice, V.; Guerrini, A.; Silveira, F.; Cecchinato, M.; Catelli, E. Molecular characterization of the meq gene of Marek’s disease viruses detected in unvaccinated backyard chickens reveals the circulation of low- and high-virulence strains. Poult. Sci., 2019, 98(8), 3130-3137.
[http://dx.doi.org/10.3382/ps/pez095] [PMID: 30850833]
[10]
Philchenkov, A.; Miura, K. The IAP protein family, SMAC mimetics and cancer treatment. Crit. Rev. Oncog., 2016, 21(3-4), 185-202.
[http://dx.doi.org/10.1615/CritRevOncog.2016017032] [PMID: 27915971]
[11]
Chesi, M.; Mirza, N.N.; Garbitt, V.M.; Sharik, M.E.; Dueck, A.C.; Asmann, Y.W.; Akhmetzyanova, I.; Kosiorek, H.E.; Calcinotto, A.; Riggs, D.L.; Keane, N.; Ahmann, G.J.; Morrison, K.M.; Fonseca, R.; Lacy, M.Q.; Dingli, D.; Kumar, S.K.; Ailawadhi, S.; Dispenzieri, A.; Buadi, F.; Gertz, M.A.; Reeder, C.B.; Lin, Y.; Chanan-Khan, A.A.; Stewart, A.K.; Fooksman, D.; Bergsagel, P.L. IAP antagonists induce anti-tumor immunity in multiple myeloma. Nat. Med., 2016, 22(12), 1411-1420.
[http://dx.doi.org/10.1038/nm.4229] [PMID: 27841872]
[12]
Ren, K.; Chong, D.; Ma, L; Zhang, Z; Zhao, S. [Effects of LCL161, a SMAC mimetic on the proliferation and apoptosis in hepatocellular carcinoma cells]. Zhong Nan Da Xue Xue Bao Yi Xue Ban, 2016, 41(9), 898-904.
[13]
Gerges, S.; Rohde, K.; Fulda, S. Cotreatment with Smac mimetics and demethylating agents induces both apoptotic and necroptotic cell death pathways in acute lymphoblastic leukemia cells. Cancer Lett., 2016, 375(1), 127-132.
[http://dx.doi.org/10.1016/j.canlet.2016.02.040] [PMID: 26944210]
[14]
Yang, C.; Wang, H.; Zhang, B.; Chen, Y.; Zhang, Y.; Sun, X.; Xiao, G.; Nan, K.; Ren, H.; Qin, S. LCL161 increases paclitaxel-induced apoptosis by degrading cIAP1 and cIAP2 in NSCLC. J.Journal of experimental & clinical cancer research. CR (East Lansing Mich.), 2016, 35(1), 158.
[15]
Jin, G.; Lan, Y.; Han, F.; Sun, Y.; Liu, Z.; Zhang, M.; Liu, X.; Zhang, X.; Hu, J.; Liu, H.; Wang, B. Smac mimetic‑induced caspase‑independent necroptosis requires RIP1 in breast cancer. Mol. Med. Rep., 2016, 13(1), 359-366.
[http://dx.doi.org/10.3892/mmr.2015.4542] [PMID: 26573429]
[16]
Yousefi, H. Long noncoding RNAs and exosomal lncRNAs: classification, and mechanisms in breast cancer metastasis and drug resistance. Oncogene, 2020, 39(5), 953-974.
[17]
Weisberg, E.; Ray, A.; Barrett, R.; Nelson, E.; Christie, A.L.; Porter, D.; Straub, C.; Zawel, L.; Daley, J.F.; Lazo-Kallanian, S.; Stone, R.; Galinsky, I.; Frank, D.; Kung, A.L.; Griffin, J.D. Smac mimetics: implications for enhancement of targeted therapies in leukemia. Leukemia, 2010, 24(12), 2100-2109.
[http://dx.doi.org/10.1038/leu.2010.212] [PMID: 20844561]
[18]
Yao, W.; Lin, Z. Delicaflavone induces ROS-mediated apoptosis and inhibits PI3K/AKT/mTOR and Ras/MEK/Erk signaling pathways in colorectal cancer cells. J. Biochem. Pharmacol., 2019. 113680.
[19]
Al-Alem, L.F.; Baker, A.T.; Pandya, U.M.; Eisenhauer, E.L.; Rueda, B.R. Understanding and targeting apoptotic pathways in ovarian cancer. Cancers (Basel), 2019, 11(11)E1631
[http://dx.doi.org/10.3390/cancers11111631] [PMID: 31652965]
[20]
Vanden Berghe, T.; Kaiser, W.J.; Bertrand, M.J.; Vandenabeele, P. Molecular crosstalk between apoptosis, necroptosis, and survival signaling. Mol. Cell. Oncol., 2015, 2(4)e975093
[http://dx.doi.org/10.4161/23723556.2014.975093] [PMID: 27308513]
[21]
Ramakrishnan, V.; Painuly, U.; Kimlinger, T.; Haug, J.; Rajkumar, S.V.; Kumar, S. Inhibitor of apoptosis proteins as therapeutic targets in multiple myeloma. Leukemia, 2014, 28(7), 1519-1528.
[http://dx.doi.org/10.1038/leu.2014.2] [PMID: 24402161]
[22]
Chen, C.W.; Li, Y.; Hu, S.; Zhou, W.; Meng, Y.; Li, Z.; Zhang, Y.; Sun, J.; Bo, Z.; DePamphilis, M.L.; Yen, Y.; Han, Z.; Zhu, W. DHS (trans-4,4′-dihydroxystilbene) suppresses DNA replication and tumor growth by inhibiting RRM2 (ribonucleotide reductase regulatory subunit M2). Oncogene, 2019, 38(13), 2364-2379.
[http://dx.doi.org/10.1038/s41388-018-0584-6] [PMID: 30518875]
[23]
Wang, Y.; Zhi, Q.; Ye, Q.; Zhou, C.; Zhang, L.; Yan, W.; Wu, Q.; Zhang, D.; Li, P.; Huo, K. SCYL1-BP1 affects cell cycle arrest in human hepatocellular carcinoma cells via Cyclin F and RRM2. Anticancer. Agents Med. Chem., 2016, 16(4), 440-446.
[http://dx.doi.org/10.2174/1871520615666150518093814] [PMID: 25980818]
[24]
Lu, A.G.; Feng, H.; Wang, P.X.; Han, D.P.; Chen, X.H.; Zheng, M.H. Emerging roles of the ribonucleotide reductase M2 in colorectal cancer and ultraviolet-induced DNA damage repair. World J. Gastroenterol., 2012, 18(34), 4704-4713.
[http://dx.doi.org/10.3748/wjg.v18.i34.4704] [PMID: 23002339]
[25]
Gautam, A.; Bepler, G. Suppression of lung tumor formation by the regulatory subunit of ribonucleotide reductase. Cancer Res., 2006, 66(13), 6497-6502.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-4462] [PMID: 16818620]
[26]
Fatkhutdinov, N.; Sproesser, K.; Krepler, C.; Liu, Q.; Brafford, P.A.; Herlyn, M.; Aird, K.M.; Zhang, R. Targeting RRM2 and mutant BRAF is a novel combinatorial strategy for melanoma. Mol. Cancer Res., 2016, 14(9), 767-775.
[http://dx.doi.org/10.1158/1541-7786.MCR-16-0099] [PMID: 27297629]
[27]
Zheng, S.; Wang, X.; Weng, Y.H.; Jin, X.; Ji, J.L.; Guo, L.; Hu, B.; Liu, N.; Cheng, Q.; Zhang, J.; Bai, H.; Yang, T.; Xia, X.H.; Zhang, H.Y.; Gao, S.; Huang, Y. siRNA knockdown of RRM2 effectively suppressed pancreatic tumor growth alone or synergistically with doxorubicin. J. Mol. Ther. Nucleic Acids, 2018, 12, 805-816.
[28]
Burton, T.R.; Kashour, T.; Wright, J.A.; Amara, F.M. Cellular signaling pathways affect the function of ribonucleotide reductase mRNA binding proteins: mRNA stabilization, drug resistance, and malignancy (Review). Int. J. Oncol., 2003, 22(1), 21-31.
[http://dx.doi.org/10.3892/ijo.22.1.21] [PMID: 12469181]
[29]
Wang, A.; Zhao, C.; Liu, X.; Su, W.; Duan, G.; Xie, Z.; Chu, S.; Gao, Y. Knockdown of TBRG4 affects tumorigenesis in human H1299 lung cancer cells by regulating DDIT3, CAV1 and RRM2. Oncol. Lett., 2018, 15(1), 121-128.
[PMID: 29387213]
[30]
Ferrandina, G.; Mey, V.; Nannizzi, S.; Ricciardi, S.; Petrillo, M.; Ferlini, C.; Danesi, R.; Scambia, G.; Del Tacca, M. Expression of nucleoside transporters, deoxycitidine kinase, ribonucleotide reductase regulatory subunits, and gemcitabine catabolic enzymes in primary ovarian cancer. Cancer Chemother. Pharmacol., 2010, 65(4), 679-686.
[http://dx.doi.org/10.1007/s00280-009-1073-y] [PMID: 19639316]
[31]
Satow, R.; Shitashige, M.; Kanai, Y.; Takeshita, F.; Ojima, H.; Jigami, T.; Honda, K.; Kosuge, T.; Ochiya, T.; Hirohashi, S.; Yamada, T. Combined functional genome survey of therapeutic targets for hepatocellular carcinoma. Clin. Cancer Res., 2010, 16(9), 2518-2528.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-2214] [PMID: 20388846]
[32]
Zuckerman, J.E.; Hsueh, T.; Koya, R.C.; Davis, M.E.; Ribas, A. siRNA knockdown of ribonucleotide reductase inhibits melanoma cell line proliferation alone or synergistically with temozolomide. J. Invest. Dermatol., 2011, 131(2), 453-460.
[http://dx.doi.org/10.1038/jid.2010.310] [PMID: 20944646]
[33]
Grade, M.; Hummon, A.B.; Camps, J.; Emons, G.; Spitzner, M.; Gaedcke, J.; Hoermann, P.; Ebner, R.; Becker, H.; Difilippantonio, M.J.; Ghadimi, B.M.; Beissbarth, T.; Caplen, N.J.; Ried, T. A genomic strategy for the functional validation of colorectal cancer genes identifies potential therapeutic targets. Int. J. Cancer, 2011, 128(5), 1069-1079.
[http://dx.doi.org/10.1002/ijc.25453] [PMID: 20473941]
[34]
Kittler, R.; Putz, G.; Pelletier, L.; Poser, I.; Heninger, A.K.; Drechsel, D.; Fischer, S.; Konstantinova, I.; Habermann, B.; Grabner, H.; Yaspo, M.L.; Himmelbauer, H.; Korn, B.; Neugebauer, K.; Pisabarro, M.T.; Buchholz, F. An endoribonuclease-prepared siRNA screen in human cells identifies genes essential for cell division. Nature, 2004, 432(7020), 1036-1040.
[http://dx.doi.org/10.1038/nature03159] [PMID: 15616564]
[35]
Liu, X.; Zhou, B.; Xue, L.; Yen, F.; Chu, P.; Un, F.; Yen, Y. Ribonucleotide reductase subunits M2 and p53R2 are potential biomarkers for metastasis of colon cancer. J. Clin. Colorectal Cancer, 2007, 6(5), 374-381.
[36]
Liang, W.H.; Li, N.; Yuan, Z.Q.; Qian, X.L.; Wang, Z.H. DSCAM-AS1 promotes tumor growth of breast cancer by reducing miR-204-5p and up-regulating RRM2. Mol. Carcinog., 2019, 58(4), 461-473.
[http://dx.doi.org/10.1002/mc.22941] [PMID: 30457164]
[37]
Fang, Z.; Gong, C.; Liu, H.; Zhang, X.; Mei, L.; Song, M.; Qiu, L.; Luo, S.; Zhu, Z.; Zhang, R.; Gu, H.; Chen, X. E2F1 promote the aggressiveness of human colorectal cancer by activating the ribonucleotide reductase small subunit M2. Biochem. Biophys. Res. Commun., 2015, 464(2), 407-415.
[http://dx.doi.org/10.1016/j.bbrc.2015.06.103] [PMID: 26093293]
[38]
Zhang, H.; Liu, X.; Warden, C.D.; Huang, Y.; Loera, S.; Xue, L.; Zhang, S.; Chu, P.; Zheng, S.; Yen, Y. Prognostic and therapeutic significance of ribonucleotide reductase small subunit M2 in estrogen-negative breast cancers. BMC Cancer, 2014, 14, 664.
[http://dx.doi.org/10.1186/1471-2407-14-664] [PMID: 25213022]
[39]
Lee, B.; Ha, S.Y.; Song, D.H.; Lee, H.W.; Cho, S.Y.; Park, C.K. High expression of ribonucleotide reductase subunit M2 correlates with poor prognosis of hepatocellular carcinoma. Gut Liver, 2014, 8(6), 662-668.
[http://dx.doi.org/10.5009/gnl13392] [PMID: 25368754]
[40]
Mah, V.; Alavi, M.; Márquez-Garbán, D.C.; Maresh, E.L.; Kim, S.R.; Horvath, S.; Bagryanova, L.; Huerta-Yepez, S.; Chia, D.; Pietras, R.; Goodglick, L. Ribonucleotide reductase subunit M2 predicts survival in subgroups of patients with non-small cell lung carcinoma: effects of gender and smoking status. PLoS One, 2015, 10(5)e0127600
[http://dx.doi.org/10.1371/journal.pone.0127600] [PMID: 26001082]
[41]
Osako, Y.; Yoshino, H.; Sakaguchi, T.; Sugita, S.; Yonemori, M.; Nakagawa, M.; Enokida, H. Potential tumor‑suppressive role of microRNA‑99a‑3p in sunitinib‑resistant renal cell carcinoma cells through the regulation of RRM2. Int. J. Oncol., 2019, 54(5), 1759-1770.
[http://dx.doi.org/10.3892/ijo.2019.4736] [PMID: 30816432]
[42]
Lu, H.; Lu, S.; Yang, D.; Zhang, L.; Ye, J.; Li, M.; Hu, W. MiR-20a-5p regulates gemcitabine chemosensitivity by targeting RRM2 in pancreatic cancer cells and serves as a predictor for gemcitabine-based chemotherapy. J. Biosci. Rep., 2019, 39(5)
[http://dx.doi.org/10.1042/BSR20181374]
[43]
Sun, H.; Yang, B.; Zhang, H.; Song, J.; Zhang, Y.; Xing, J.; Yang, Z.; Wei, C.; Xu, T.; Yu, Z.; Xu, Z.; Hou, M.; Ji, M.; Zhang, Y. RRM2 is a potential prognostic biomarker with functional significance in glioma. Int. J. Biol. Sci., 2019, 15(3), 533-543.
[http://dx.doi.org/10.7150/ijbs.30114] [PMID: 30745840]
[44]
Liu; Jiamin, P.; Yayun, Z.; Bei, X.; Jianchao, W. Silencing RRM2 inhibits multiple myeloma by targeting the Wnt/β catenin signaling pathway. J. Mol. Medic. Rep., 2019, 20(3), 2159-2166.
[45]
Susin, S.A.; Lorenzo, H.K.; Zamzami, N.; Marzo, I.; Snow, B.E.; Brothers, G.M.; Mangion, J.; Jacotot, E.; Costantini, P.; Loeffler, M.; Larochette, N.; Goodlett, D.R.; Aebersold, R.; Siderovski, D.P.; Penninger, J.M.; Kroemer, G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature, 1999, 397(6718), 441-446.
[http://dx.doi.org/10.1038/17135] [PMID: 9989411]
[46]
Miramar, M.D.; Costantini, P.; Ravagnan, L.; Saraiva, L.M.; Haouzi, D.; Brothers, G.; Penninger, J.M.; Peleato, M.L.; Kroemer, G.; Susin, S.A. NADH oxidase activity of mitochondrial apoptosis-inducing factor. J. Biol. Chem., 2001, 276(19), 16391-16398.
[http://dx.doi.org/10.1074/jbc.M010498200] [PMID: 11278689]
[47]
Li, L.Y.; Luo, X.; Wang, X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature, 2001, 412(6842), 95-99.
[http://dx.doi.org/10.1038/35083620] [PMID: 11452314]
[48]
Enari, M.; Sakahira, H.; Yokoyama, H.; Okawa, K.; Iwamatsu, A.; Nagata, S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature, 1998, 391(6662), 43-50.
[http://dx.doi.org/10.1038/34112] [PMID: 9422506]
[49]
Ingham, M.; Schwartz, G.K. Cell-cycle therapeutics come of age. J. Clin. Oncol., 2017, 35(25), 2949-2959.
[http://dx.doi.org/10.1200/JCO.2016.69.0032] [PMID: 28580868]
[50]
Yu, Q.; Geng, Y.; Sicinski, P. Specific protection against breast cancers by cyclin D1 ablation. Nature, 2001, 411(6841), 1017-1021.
[http://dx.doi.org/10.1038/35082500] [PMID: 11429595]
[51]
Yu, Q.; Sicinska, E.; Geng, Y.; Ahnström, M.; Zagozdzon, A.; Kong, Y.; Gardner, H.; Kiyokawa, H.; Harris, L.N.; Stål, O.; Sicinski, P. Requirement for CDK4 kinase function in breast cancer. Cancer Cell, 2006, 9(1), 23-32.
[http://dx.doi.org/10.1016/j.ccr.2005.12.012] [PMID: 16413469]
[52]
Zhu, S.; Mott, R.T.; Fry, E.A.; Taneja, P.; Kulik, G.; Sui, G.; Inoue, K. Cooperation between Dmp1 loss and cyclin D1 overexpression in breast cancer. Am. J. Pathol., 2013, 183(4), 1339-1350.
[http://dx.doi.org/10.1016/j.ajpath.2013.06.027] [PMID: 23938323]
[53]
Chen, F.; Liu, C.; Zhang, J.; Xu, W.; Zhang, Y. Progress of CDK4/6 inhibitor palbociclib in the treatment of cancer. Anticancer. Agents Med. Chem., 2018, 18(9), 1241-1251.
[http://dx.doi.org/10.2174/1871521409666170412123500] [PMID: 28403773]
[54]
Schwartz, G.K.; Shah, M.A. Targeting the cell cycle: a new approach to cancer therapy. J. Clin. Oncol., 2005, 23(36), 9408-9421.
[http://dx.doi.org/10.1200/JCO.2005.01.5594] [PMID: 16361640]
[55]
Massagué, J. G1 cell-cycle control and cancer. Nature, 2004, 432(7015), 298-306.
[http://dx.doi.org/10.1038/nature03094] [PMID: 15549091]
[56]
Brookes, S.; Gagrica, S.; Sanij, E.; Rowe, J.; Gregory, F.J.; Hara, E.; Peters, G. Evidence for a CDK4-dependent checkpoint in a conditional model of cellular senescence. Cell Cycle, 2015, 14(8), 1164-1173.
[http://dx.doi.org/10.1080/15384101.2015.1010866] [PMID: 25695870]
[57]
Finn, R.S.; Dering, J.; Conklin, D.; Kalous, O.; Cohen, D.J.; Desai, A.J.; Ginther, C.; Atefi, M.; Chen, I.; Fowst, C.; Los, G.; Slamon, D.J. PD 0332991, a selective cyclin D kinase 4/6 inhibitor, preferentially inhibits proliferation of luminal estrogen receptor-positive human breast cancer cell lines in vitro. Breast Cancer Res., 2009, 11(5), R77.
[http://dx.doi.org/10.1186/bcr2419] [PMID: 19874578]
[58]
Wardell, S.E.; Ellis, M.J.; Alley, H.M.; Eisele, K.; VanArsdale, T.; Dann, S.G.; Arndt, K.T.; Primeau, T.; Griffin, E.; Shao, J.; Crowder, R.; Lai, J.P.; Norris, J.D.; McDonnell, D.P.; Li, S. Efficacy of SERD/SERM hybrid-CDK4/6 inhibitor combinations in models of endocrine therapy-resistant breast cancer. Clin. Cancer Res., 2015, 21(22), 5121-5130.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-0360] [PMID: 25991817]
[59]
Malorni, L.; Curigliano, G.; Minisini, A.M.; Cinieri, S.; Tondini, C.A.; D’Hollander, K.; Arpino, G.; Bernardo, A.; Martignetti, A.; Criscitiello, C.; Puglisi, F.; Pestrin, M.; Sanna, G.; Moretti, E.; Risi, E.; Biagioni, C.; McCartney, A.; Boni, L.; Buyse, M.; Migliaccio, I.; Biganzoli, L.; Di Leo, A. Palbociclib as single agent or in combination with the endocrine therapy received before disease progression for estrogen receptor-positive, HER2-negative metastatic breast cancer: TREnd trial. Ann. Oncol., 2018, 29(8), 1748-1754.
[http://dx.doi.org/10.1093/annonc/mdy214] [PMID: 29893790]
[60]
Haraguchi, N.; Inoue, H.; Tanaka, F.; Mimori, K.; Utsunomiya, T.; Sasaki, A.; Mori, M. Cancer stem cells in human gastrointestinal cancers. Hum. Cell, 2006, 19(1), 24-29.
[http://dx.doi.org/10.1111/j.1749-0774.2005.00004.x] [PMID: 16643604]
[61]
Corbeil, D.; Röper, K.; Hellwig, A.; Tavian, M.; Miraglia, S.; Watt, S.M.; Simmons, P.J.; Peault, B.; Buck, D.W.; Huttner, W.B. The human AC133 hematopoietic stem cell antigen is also expressed in epithelial cells and targeted to plasma membrane protrusions. J. Biol. Chem., 2000, 275(8), 5512-5520.
[http://dx.doi.org/10.1074/jbc.275.8.5512] [PMID: 10681530]
[62]
Corbeil, D.; Röper, K.; Fargeas, C.A.; Joester, A.; Huttner, W.B. Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic, 2001, 2(2), 82-91.
[http://dx.doi.org/10.1034/j.1600-0854.2001.020202.x] [PMID: 11247306]
[63]
Wang, Y.K.; Zhu, Y.L.; Qiu, F.M.; Zhang, T.; Chen, Z.G.; Zheng, S.; Huang, J. Activation of Akt and MAPK pathways enhances the tumorigenicity of CD133+ primary colon cancer cells. Carcinogenesis, 2010, 31(8), 1376-1380.
[http://dx.doi.org/10.1093/carcin/bgq120] [PMID: 20530554]
[64]
Shmelkov, S.V.; Butler, J.M.; Hooper, A.T.; Hormigo, A.; Kushner, J.; Milde, T.; St Clair, R.; Baljevic, M.; White, I.; Jin, D.K.; Chadburn, A.; Murphy, A.J.; Valenzuela, D.M.; Gale, N.W.; Thurston, G.; Yancopoulos, G.D.; D’Angelica, M.; Kemeny, N.; Lyden, D.; Rafii, S. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J. Clin. Invest., 2008, 118(6), 2111-2120.
[65]
Bidlingmaier, S.; Zhu, X.; Liu, B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J. Mol. Med. (Berl.), 2008, 86(9), 1025-1032.
[http://dx.doi.org/10.1007/s00109-008-0357-8] [PMID: 18535813]
[66]
Song, J.; Zhang, J.; Wang, J.; Cao, Z.; Wang, J.; Guo, X.; Dong, W. β1 integrin modulates tumor growth and apoptosis of human colorectal cancer. Oncol. Rep., 2014, 32(1), 302-308.
[http://dx.doi.org/10.3892/or.2014.3168] [PMID: 24807392]
[67]
Song, J.; Zhang, J.; Wang, J.; Wang, J.; Guo, X.; Dong, W. β1 integrin mediates colorectal cancer cell proliferation and migration through regulation of the Hedgehog pathway. Tumour Biol., 2015, 36(3), 2013-2021.
[http://dx.doi.org/10.1007/s13277-014-2808-x] [PMID: 25387809]
[68]
Kim, J.Y.; Beart, R.W.; Shibata, D. Stability of colon stem cell methylation after neo-adjuvant therapy in a patient with attenuated familial adenomatous polyposis. BMC Gastroenterol., 2005, 5(1), 19-19.
[http://dx.doi.org/10.1186/1471-230X-5-19] [PMID: 15941485]
[69]
Yang, Z.; Zhou, X.; Liu, Y.; Gong, C.; Wei, X.; Zhang, T.; Ma, D.; Gao, Q. Activation of integrin β1 mediates the increased malignant potential of ovarian cancer cells exerted by inflammatory cytokines. Anticancer. Agents Med. Chem., 2014, 14(7), 955-962.
[http://dx.doi.org/10.2174/1871520614666140613123108] [PMID: 24931361]
[70]
Alfieri, C.; Chang, L.; Zhang, Z.; Yang, J.; Maslen, S.; Skehel, M.; Barford, D. Molecular basis of APC/C regulation by the spindle assembly checkpoint. Nature, 2016, 536(7617), 431-436.
[http://dx.doi.org/10.1038/nature19083] [PMID: 27509861]
[71]
Gayyed, M.F.; El-Maqsoud, N.M.; Tawfiek, E.R.; El Gelany, S.A.; Rahman, M.F. A comprehensive analysis of CDC20 overexpression in common malignant tumors from multiple organs: its correlation with tumor grade and stage. Tumour Biol., 2016, 37(1), 749-762.
[http://dx.doi.org/10.1007/s13277-015-3808-1] [PMID: 26245990]
[72]
Hou, M.F.; Luo, C.W.; Chang, T.M.; Hung, W.C.; Chen, T.Y.; Tsai, Y.L.; Chai, C.Y.; Pan, M.R. The NuRD complex-mediated p21 suppression facilitates chemoresistance in BRCA-proficient breast cancer. Exp. Cell Res., 2017, 359(2), 458-465.
[http://dx.doi.org/10.1016/j.yexcr.2017.08.029] [PMID: 28842166]
[73]
O’Connor, L.; Strasser, A.; O’Reilly, L.A.; Hausmann, G.; Adams, J.M.; Cory, S.; Huang, D.C. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J., 1998, 17(2), 384-395.
[http://dx.doi.org/10.1093/emboj/17.2.384] [PMID: 9430630]
[74]
Wan, L.; Tan, M.; Yang, J.; Inuzuka, H.; Dai, X.; Wu, T.; Liu, J.; Shaik, S.; Chen, G.; Deng, J.; Malumbres, M.; Letai, A.; Kirschner, M.W.; Sun, Y.; Wei, W. APC(Cdc20) suppresses apoptosis through targeting Bim for ubiquitination and destruction. Dev. Cell, 2014, 29(4), 377-391.
[http://dx.doi.org/10.1016/j.devcel.2014.04.022] [PMID: 24871945]
[75]
Zheng, Y.; Lv, X.; Wang, X.; Wang, B.; Shao, X.; Huang, Y.; Shi, L.; Chen, Z.; Huang, J.; Huang, P. MiR-181b promotes chemoresistance in breast cancer by regulating Bim expression. Oncol. Rep., 2016, 35(2), 683-690.
[http://dx.doi.org/10.3892/or.2015.4417] [PMID: 26572075]
[76]
Woo, S.M.; Min, K.J.; Kwon, T.K. Melatonin-mediated Bim up-regulation and cyclooxygenase-2 (COX-2) down-regulation enhances tunicamycin-induced apoptosis in MDA-MB-231 cells. J. Pineal Res., 2015, 58(3), 310-320.
[http://dx.doi.org/10.1111/jpi.12217] [PMID: 25711465]

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