Small Molecules as Drugs to Upregulate Metastasis Suppressors in Cancer Cells

Author(s): Ka Ming Wong, Jiaxing Song, Vasu Saini, Yung H. Wong*.

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 32 , 2019

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Abstract:

It is well-recognized that the majority of cancer-related deaths is attributed to metastasis, which can arise from virtually any type of tumor. Metastasis is a complex multistep process wherein cancer cells must break away from the primary tumor, intravasate into the circulatory or lymphatic systems, extravasate, proliferate and eventually colonize secondary sites. Since these molecular processes involve the coordinated actions of numerous proteins, targeted disruptions of key players along these pathways represent possible therapeutic interventions to impede metastasis formation and reduce cancer mortality. A diverse group of proteins with demonstrated ability to inhibit metastatic colonization have been identified and they are collectively known as metastasis suppressors. Given that the metastasis suppressors are often downregulated in tumors, drug-induced re-expression or upregulation of these proteins represents a promising approach to limit metastasis. Indeed, over 40 compounds are known to exhibit efficacy in upregulating the expression of metastasis suppressors via transcriptional or post-transcriptional mechanisms, and the most promising ones are being evaluated for their translational potentials. These small molecules range from natural products to drugs in clinical use and they apparently target different molecular pathways, reflecting the diverse nature of the metastasis suppressors. In this review, we provide an overview of the different classes of compounds known to possess the ability to upregulate one or more metastasis suppressors, with an emphasis on their mechanisms of action and therapeutic potentials.

Keywords: Metastasis suppressor, small molecules, upregulation, Nm23, natural products, signaling.

[1]
Marshall, J.C.; Collins, J.; Marino, N.; Steeg, P. The Nm23-H1 metastasis suppressor as a translational target. Eur. J. Cancer, 2010, 46(7), 1278-1282.
[http://dx.doi.org/10.1016/j.ejca.2010.02.042] [PMID: 20304626]
[2]
Steeg, P.S.; Horak, C.E.; Miller, K.D. Clinical-translational approaches to the Nm23-H1 metastasis suppressor. Clin. Cancer Res., 2008, 14(16), 5006-5012.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-0238] [PMID: 18698018]
[3]
Steeg, P.S.; Bevilacqua, G.; Kopper, L.; Thorgeirsson, U.P.; Talmadge, J.E.; Liotta, L.A.; Sobel, M.E. Evidence for a novel gene associated with low tumor metastatic potential. J. Natl. Cancer Inst., 1988, 80(3), 200-204.
[http://dx.doi.org/10.1093/jnci/80.3.200] [PMID: 3346912]
[4]
Eccles, S.A.; Welch, D.R. Metastasis: recent discoveries and novel treatment strategies. Lancet, 2007, 369(9574), 1742-1757.
[http://dx.doi.org/10.1016/S0140-6736(07)60781-8] [PMID: 17512859]
[5]
Kantor, J.D.; McCormick, B.; Steeg, P.S.; Zetter, B.R. Inhibition of cell motility after nm23 transfection of human and murine tumor cells. Cancer Res., 1993, 53(9), 1971-1973.
[PMID: 8481897]
[6]
Arnaud-Dabernat, S.; Bourbon, P.M.; Dierich, A.; Le Meur, M.; Daniel, J.Y. Knockout mice as model systems for studying nm23/NDP kinase gene functions. Application to the nm23-M1 gene. J. Bioenerg. Biomembr., 2003, 35(1), 19-30.
[http://dx.doi.org/10.1023/A:1023561821551] [PMID: 12848338]
[7]
Boissan, M.; Wendum, D.; Arnaud-Dabernat, S.; Munier, A.; Debray, M.; Lascu, I.; Daniel, J.Y.; Lacombe, M.L. Increased lung metastasis in transgenic NM23-Null/SV40 mice with hepatocellular carcinoma. J. Natl. Cancer Inst., 2005, 97(11), 836-845.
[http://dx.doi.org/10.1093/jnci/dji143] [PMID: 15928304]
[8]
MacDonald, N.J.; de la Rosa, A.; Steeg, P.S. The potential roles of nm23 in cancer metastasis and cellular differentiation. Eur. J. Cancer, 1995, 31A(7-8), 1096-1100.
[http://dx.doi.org/10.1016/0959-8049(95)00152-9] [PMID: 7576999]
[9]
Pantel, K.; Brakenhoff, R.H.; Brandt, B. Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat. Rev. Cancer, 2008, 8(5), 329-340.
[http://dx.doi.org/10.1038/nrc2375] [PMID: 18404148]
[10]
Cui, R.X.; Liu, N.; He, Q.M.; Li, W.F.; Huang, B.J.; Sun, Y.; Tang, L.L.; Chen, M.; Jiang, N.; Chen, L.; Yun, J.P.; Zeng, J.; Guo, Y.; Wang, H.Y.; Ma, J. Low BRMS1 expression promotes nasopharyngeal carcinoma metastasis in vitro and in vivo and is associated with poor patient survival. BMC Cancer, 2012, 12, 376.
[http://dx.doi.org/10.1186/1471-2407-12-376] [PMID: 22931099]
[11]
Ullmannova, V.; Popescu, N.C. Expression profile of the tumor suppressor genes DLC-1 and DLC-2 in solid tumors. Int. J. Oncol., 2006, 29(5), 1127-1132.
[http://dx.doi.org/10.3892/ijo.29.5.1127] [PMID: 17016643]
[12]
Yonemura, Y.; Endou, Y.; Kimura, K.; Fushida, S.; Bandou, E.; Taniguchi, K.; Kinoshita, K.; Ninomiya, I.; Sugiyama, K.; Heizmann, C.W.; Schafer, B.W.; Sasaki, T. Inverse expression of S100A4 and E-cadherin is associated with metastatic potential in gastric cancer. Clin. Cancer Res., 2000, 6(11), 4234-4242.
[PMID: 11106237]
[13]
Guo, X.; Friess, H.; Graber, H.U.; Kashiwagi, M.; Zimmermann, A.; Korc, M.; Büchler, M.W. KAI1 expression is up-regulated in early pancreatic cancer and decreased in the presence of metastases. Cancer Res., 1996, 56(21), 4876-4880.
[PMID: 8895737]
[14]
Guan-Zhen, Y.; Ying, C.; Can-Rong, N.; Guo-Dong, W.; Jian-Xin, Q.; Jie-Jun, W. Reduced protein expression of metastasis-related genes (nm23, KISS1, KAI1 and p53) in lymph node and liver metastases of gastric cancer. Int. J. Exp. Pathol., 2007, 88(3), 175-183.
[http://dx.doi.org/10.1111/j.1365-2613.2006.00510.x] [PMID: 17504447]
[15]
Sun, B.; Chu, D.; Li, W.; Chu, X.; Li, Y.; Wei, D.; Li, H. Decreased expression of NDRG1 in glioma is related to tumor progression and survival of patients. J. Neurooncol., 2009, 94(2), 213-219.
[http://dx.doi.org/10.1007/s11060-009-9859-7] [PMID: 19337694]
[16]
Fu, Z.; Kitagawa, Y.; Shen, R.; Shah, R.; Mehra, R.; Rhodes, D.; Keller, P.J.; Mizokami, A.; Dunn, R.; Chinnaiyan, A.M.; Yao, Z.; Keller, E.T. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate, 2006, 66(3), 248-256.
[http://dx.doi.org/10.1002/pros.20319] [PMID: 16175585]
[17]
Shoushtari, A.N.; Szmulewitz, R.Z.; Rinker-Schaeffer, C.W. Metastasis-suppressor genes in clinical practice: lost in translation? Nat. Rev. Clin. Oncol., 2011, 8(6), 333-342.
[http://dx.doi.org/10.1038/nrclinonc.2011.65] [PMID: 21522123]
[18]
Stafford, L.J.; Vaidya, K.S.; Welch, D.R. Metastasis suppressors genes in cancer. Int. J. Biochem. Cell Biol., 2008, 40(5), 874-891.
[http://dx.doi.org/10.1016/j.biocel.2007.12.016] [PMID: 18280770]
[19]
Khan, I.; Steeg, P.S. Metastasis suppressors: functional pathways. Lab. Invest., 2018, 98(2), 198-210.
[PMID: 28967874]
[20]
Thiolloy, S.; Rinker-Schaeffer, C.W. Thinking outside the box: using metastasis suppressors as molecular tools. Semin. Cancer Biol., 2011, 21(2), 89-98.
[http://dx.doi.org/10.1016/j.semcancer.2010.12.008] [PMID: 21147228]
[21]
Shi, J.; Liu, H.; Yao, F.; Zhong, C.; Zhao, H. Upregulation of mediator MED23 in non-small-cell lung cancer promotes the growth, migration, and metastasis of cancer cells. Tumour Biol., 2014, 35(12), 12005-12013.
[http://dx.doi.org/10.1007/s13277-014-2499-3] [PMID: 25273169]
[22]
Wang, L.; Pan, Y.; Dai, J.L. Evidence of MKK4 pro-oncogenic activity in breast and pancreatic tumors. Oncogene, 2004, 23(35), 5978-5985.
[http://dx.doi.org/10.1038/sj.onc.1207802] [PMID: 15184866]
[23]
Cho, H.J.; Baek, K.E.; Park, S.M.; Kim, I.K.; Nam, I.K.; Choi, Y.L.; Park, S.H. Im, M.J.; Choi, J.; Ryu, J.; Kim, J.W.; Lee, C.W.; Kang, S.S.; Yoo, J. RhoGDI2 confers gastric cancer cells resistance against cisplatin-induced apoptosis by upregulation of Bcl-2 expression. Cancer Lett., 2011, 311(1), 48-56.
[http://dx.doi.org/10.1016/j.canlet.2011.06.024] [PMID: 21752536]
[24]
Junn, E.; Han, S.H. Im, J.Y.; Yang, Y.; Cho, E.W.; Um, H.D.; Kim, D.K.; Lee, K.W.; Han, P.L.; Rhee, S.G.; Choi, I. Vitamin D3 up-regulated protein 1 mediates oxidative stress via suppressing the thioredoxin function. J. Immunol., 2000, 164(12), 6287-6295.
[http://dx.doi.org/10.4049/jimmunol.164.12.6287] [PMID: 10843682]
[25]
Lee, K.N.; Kang, H.S.; Jeon, J.H.; Kim, E.M.; Yoon, S.R.; Song, H.; Lyu, C.Y.; Piao, Z.H.; Kim, S.U.; Han, Y.H.; Song, S.S.; Lee, Y.H.; Song, K.S.; Kim, Y.M.; Yu, D.Y.; Choi, I. VDUP1 is required for the development of natural killer cells. Immunity, 2005, 22(2), 195-208.
[http://dx.doi.org/10.1016/j.immuni.2004.12.012] [PMID: 15723808]
[26]
Chen, H.C.; Wang, L.; Banerjee, S. Isolation and characterization of the promoter region of human nm23-H1, a metastasis suppressor gene. Oncogene, 1994, 9(10), 2905-2912.
[PMID: 8084595]
[27]
Okada, K.; Urano, T.; Baba, H.; Furukawa, K.; Furukawa, K.; Shiku, H. Independent and differential expression of two isotypes of human Nm23: analysis of the promoter regions of the nm23-H1 and H2 genes. Oncogene, 1996, 13(9), 1937-1943.
[PMID: 8934540]
[28]
Li, Y.; Song, J.; Tong, Y.; Chung, S.K.; Wong, Y.H. RGS19 upregulates Nm23-H1/2 metastasis suppressors by transcriptional activation via the cAMP/PKA/CREB pathway. Oncotarget, 2017, 8(41), 69945-69960.
[http://dx.doi.org/10.18632/oncotarget.19509] [PMID: 29050254]
[29]
Ouatas, T.; Halverson, D.; Steeg, P.S. Dexamethasone and medroxyprogesterone acetate elevate Nm23-H1 metastasis suppressor gene expression in metastatic human breast carcinoma cells: new uses for old compounds. Clin. Cancer Res., 2003, 9(10 Pt 1), 3763-3772.
[PMID: 14506169]
[30]
Palmieri, D.; Halverson, D.O.; Ouatas, T.; Horak, C.E.; Salerno, M.; Johnson, J.; Figg, W.D.; Hollingshead, M.; Hursting, S.; Berrigan, D.; Steinberg, S.M.; Merino, M.J.; Steeg, P.S. Medroxyprogesterone acetate elevation of Nm23-H1 metastasis suppressor expression in hormone receptor-negative breast cancer. J. Natl. Cancer Inst., 2005, 97(9), 632-642.
[http://dx.doi.org/10.1093/jnci/dji111] [PMID: 15870434]
[31]
Lin, K.H.; Shieh, H.Y.; Hsu, H.C. Negative regulation of the antimetastatic gene Nm23-H1 by thyroid hormone receptors. Endocrinology, 2000, 141(7), 2540-2547.
[http://dx.doi.org/10.1210/endo.141.7.7570] [PMID: 10875256]
[32]
Zhang, L.; Li, L.; Wei, H.; Guo, L.; Ai, C.; Xu, H.; Wu, Z.; Zhou, Q. Transcriptional factor FOXO3 negatively regulates the expression of nm23-H1 in non-small cell lung cancer. Thorac. Cancer, 2016, 7(1), 9-16.
[http://dx.doi.org/10.1111/1759-7714.12260] [PMID: 26816534]
[33]
Chang, Y.W.; Chiu, C.F.; Lee, K.Y.; Hong, C.C.; Wang, Y.Y.; Cheng, C.C.; Jan, Y.H.; Huang, M.S.; Hsiao, M.; Ma, J.T.; Su, J.L. CARMA3 represses metastasis suppressor NME2 to promote lung cancer stemness and metastasis. Am. J. Respir. Crit. Care Med., 2015, 192(1), 64-75.
[http://dx.doi.org/10.1164/rccm.201411-1957OC] [PMID: 25906011]
[34]
Iiizumi, M.; Liu, W.; Pai, S.K.; Furuta, E.; Watabe, K. Drug development against metastasis-related genes and their pathways: a rationale for cancer therapy. Biochim. Biophys. Acta, 2008, 1786(2), 87-104.
[PMID: 18692117]
[35]
Yu, H.G.; Huang, J.A.; Yang, Y.N.; Huang, H.; Luo, H.S.; Yu, J.P.; Meier, J.J.; Schrader, H.; Bastian, A.; Schmidt, W.E.; Schmitz, F. The effects of acetylsalicylic acid on proliferation, apoptosis, and invasion of cyclooxygenase-2 negative colon cancer cells. Eur. J. Clin. Invest., 2002, 32(11), 838-846.
[http://dx.doi.org/10.1046/j.1365-2362.2002.01080.x] [PMID: 12423325]
[36]
Natarajan, K.; Mori, N.; Artemov, D.; Bhujwalla, Z.M. Exposure of human breast cancer cells to the anti-inflammatory agent indomethacin alters choline phospholipid metabolites and Nm23 expression. Neoplasia, 2002, 4(5), 409-416.
[http://dx.doi.org/10.1038/sj.neo.7900252] [PMID: 12192599]
[37]
Chen, C.; Li, G.; Liao, W.; Wu, J.; Liu, L.; Ma, D.; Zhou, J.; Elbekai, R.H.; Edin, M.L.; Zeldin, D.C.; Wang, D.W. Selective inhibitors of CYP2J2 related to terfenadine exhibit strong activity against human cancers in vitro and in vivo. J. Pharmacol. Exp. Ther., 2009, 329(3), 908-918.
[http://dx.doi.org/10.1124/jpet.109.152017] [PMID: 19289568]
[38]
Yang, L.; Huang, Y.; Porta, R.; Yanagisawa, K.; Gonzalez, A.; Segi, E.; Johnson, D.H.; Narumiya, S.; Carbone, D.P. Host and direct antitumor effects and profound reduction in tumor metastasis with selective EP4 receptor antagonism. Cancer Res., 2006, 66(19), 9665-9672.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-1271] [PMID: 17018624]
[39]
Chell, S.D.; Witherden, I.R.; Dobson, R.R.; Moorghen, M.; Herman, A.A.; Qualtrough, D.; Williams, A.C.; Paraskeva, C. Increased EP4 receptor expression in colorectal cancer progression promotes cell growth and anchorage independence. Cancer Res., 2006, 66(6), 3106-3113.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-3702] [PMID: 16540660]
[40]
Kundu, N.; Ma, X.; Holt, D.; Goloubeva, O.; Ostrand-Rosenberg, S.; Fulton, A.M. Antagonism of the prostaglandin E receptor EP4 inhibits metastasis and enhances NK function. Breast Cancer Res. Treat., 2009, 117(2), 235-242.
[http://dx.doi.org/10.1007/s10549-008-0180-5] [PMID: 18792778]
[41]
Rothwell, P.M.; Wilson, M.; Price, J.F.; Belch, J.F.F.; Meade, T.W.; Mehta, Z. Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. Lancet, 2012, 379(9826), 1591-1601.
[http://dx.doi.org/10.1016/S0140-6736(12)60209-8] [PMID: 22440947]
[42]
Shi, C.; Zhang, N.; Feng, Y.; Cao, J.; Chen, X.; Liu, B. Aspirin inhibits IKK-β-mediated prostate cancer cell invasion by targeting matrix metalloproteinase-9 and urokinase-type plasminogen activator. Cell. Physiol. Biochem., 2017, 41(4), 1313-1324.
[http://dx.doi.org/10.1159/000464434] [PMID: 28278500]
[43]
Xin, X.; Majumder, M.; Girish, G.V.; Mohindra, V.; Maruyama, T.; Lala, P.K. Targeting COX-2 and EP4 to control tumor growth, angiogenesis, lymphangiogenesis and metastasis to the lungs and lymph nodes in a breast cancer model. Lab. Invest., 2012, 92(8), 1115-1128.
[http://dx.doi.org/10.1038/labinvest.2012.90] [PMID: 22641101]
[44]
Meng, Z.; Cao, R.; Yang, Z.; Liu, T.; Wang, Y.; Wang, X. Inhibitor of 5-lipoxygenase, zileuton, suppresses prostate cancer metastasis by upregulating E-cadherin and paxillin. Urology, 2013, 82(6), 1452.e7-1452.e14.
[http://dx.doi.org/10.1016/j.urology.2013.08.060] [PMID: 24295266]
[45]
Rafferty, P.; Jackson, L.; Smith, R.; Holgate, S.T. Terfenadine, a potent histamine H1-receptor antagonist in the treatment of grass pollen sensitive asthma. Br. J. Clin. Pharmacol., 1990, 30(2), 229-235.
[http://dx.doi.org/10.1111/j.1365-2125.1990.tb03769.x] [PMID: 1976343]
[46]
You, J.; Chang, R.; Liu, B.; Zu, L.; Zhou, Q. Nm23-H1 was involved in regulation of KAI1 expression in high-metastatic lung cancer cells L9981. J. Thorac. Dis., 2016, 8(6), 1217-1226.
[http://dx.doi.org/10.21037/jtd.2016.04.59] [PMID: 27293840]
[47]
Jiang, J.G.; Ning, Y.G.; Chen, C.; Ma, D.; Liu, Z.J.; Yang, S.; Zhou, J.; Xiao, X.; Zhang, X.A.; Edin, M.L.; Card, J.W.; Wang, J.; Zeldin, D.C.; Wang, D.W. Cytochrome p450 epoxygenase promotes human cancer metastasis. Cancer Res., 2007, 67(14), 6665-6674.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-3643] [PMID: 17638876]
[48]
Rayner, K.; Chen, Y.X.; Hibbert, B.; White, D.; Miller, H.; Postel, E.H.; O’Brien, E.R. NM23-H2, an estrogen receptor β-associated protein, shows diminished expression with progression of atherosclerosis. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2007, 292(2), R743-R750.
[http://dx.doi.org/10.1152/ajpregu.00373.2006] [PMID: 17272673]
[49]
Ma, H.; Gollahon, L.S. ERα mediates estrogen-induced expression of the breast cancer metastasis suppressor gene BRMS1. Int. J. Mol. Sci., 2016, 17, 158.
[http://dx.doi.org/10.3390/ijms17020158]
[50]
Pike, A.C.; Brzozowski, A.M.; Hubbard, R.E.; Bonn, T.; Thorsell, A.G.; Engström, O.; Ljunggren, J.; Gustafsson, J.A.; Carlquist, M. Structure of the ligand-binding domain of oestrogen receptor beta in the presence of a partial agonist and a full antagonist. EMBO J., 1999, 18(17), 4608-4618.
[http://dx.doi.org/10.1093/emboj/18.17.4608] [PMID: 10469641]
[51]
Han, L.; Zhang, H.W.; Zhou, W.P.; Chen, G.M.; Guo, K.J. The effects of genistein on transforming growth factor-β1-induced invasion and metastasis in human pancreatic cancer cell line Panc-1 in vitro. Chin. Med. J. (Engl.), 2012, 125(11), 2032-2040.
[PMID: 22884073]
[52]
Kim, Y.S.; Choi, K.C.; Hwang, K.A. Genistein suppressed epithelial-mesenchymal transition and migration efficacies of BG-1 ovarian cancer cells activated by estrogenic chemicals via estrogen receptor pathway and downregulation of TGF-β signaling pathway. Phytomedicine, 2015, 22(11), 993-999.
[http://dx.doi.org/10.1016/j.phymed.2015.08.003] [PMID: 26407941]
[53]
El Touny, L.H.; Banerjee, P.P. Genistein induces the metastasis suppressor kangai-1 which mediates its anti-invasive effects in TRAMP cancer cells. Biochem. Biophys. Res. Commun., 2007, 361(1), 169-175.
[http://dx.doi.org/10.1016/j.bbrc.2007.07.010] [PMID: 17658479]
[54]
Christgen, M.; Bruchhardt, H.; Ballmaier, M.; Krech, T.; Länger, F.; Kreipe, H.; Lehmann, U.; Kreipe, H.; Lehmann, U. KAI1/CD82 is a novel target of estrogen receptor-mediated gene repression and downregulated in primary human breast cancer. Int. J. Cancer, 2008, 123(10), 2239-2246.
[http://dx.doi.org/10.1002/ijc.23806] [PMID: 18712725]
[55]
Marques, M.; Laflamme, L.; Benassou, I.; Cissokho, C.; Guillemette, B.; Gaudreau, L. Low levels of 3,3′-diindolylmethane activate estrogen receptor α and induce proliferation of breast cancer cells in the absence of estradiol. BMC Cancer, 2014, 14, 524.
[http://dx.doi.org/10.1186/1471-2407-14-524] [PMID: 25048790]
[56]
Lerner, A.; Grafi-Cohen, M.; Napso, T.; Azzam, N.; Fares, F. The indolic diet-derivative, 3,3′-diindolylmethane, induced apoptosis in human colon cancer cells through upregulation of NDRG1. J. Biomed. Biotechnol., 2012. 2012256178
[http://dx.doi.org/10.1155/2012/256178] [PMID: 22187533]
[57]
Lu, Y.C.; Chen, I.S.; Chou, C.T.; Huang, J.K.; Chang, H.T.; Tsai, J.Y.; Hsu, S.S.; Liao, W.C.; Wang, J.L.; Lin, K.L.; Liu, S.I.; Kuo, C.C.; Ho, C.M.; Jan, C.R. 3,3′-Diindolylmethane alters Ca2+ homeostasis and viability in MG63 human osteosarcoma cells. Basic Clin. Pharmacol. Toxicol., 2012, 110(4), 314-321.
[http://dx.doi.org/10.1111/j.1742-7843.2011.00816.x] [PMID: 21995587]
[58]
Ahmad, A.; Biersack, B.; Li, Y.; Kong, D.; Bao, B.; Schobert, R.; Padhye, S.B.; Sarkar, F.H. Targeted regulation of PI3K/Akt/mTOR/NF-κB signaling by indole compounds and their derivatives: mechanistic details and biological implications for cancer therapy. Anticancer. Agents Med. Chem., 2013, 13(7), 1002-1013.
[http://dx.doi.org/10.2174/18715206113139990078] [PMID: 23272910]
[59]
Kong, D.; Sethi, S.; Li, Y.; Chen, W.; Sakr, W.A.; Heath, E.; Sarkar, F.H. Androgen receptor splice variants contribute to prostate cancer aggressiveness through induction of EMT and expression of stem cell marker genes. Prostate, 2015, 75(2), 161-174.
[http://dx.doi.org/10.1002/pros.22901] [PMID: 25307492]
[60]
Lee, J.E.; Kim, J.H. Valproic acid inhibits the invasion of PC3 prostate cancer cells by upregulating the metastasis suppressor protein NDRG1. Genet. Mol. Biol., 2015, 38(4), 527-533.
[http://dx.doi.org/10.1590/S1415-475738420150028] [PMID: 26692161]
[61]
Semaan, S.J.; Dhamija, S.; Kim, J.; Ku, E.C.; Kauffman, A.S. Assessment of epigenetic contributions to sexually-dimorphic Kiss1 expression in the anteroventral periventricular nucleus of mice. Endocrinology, 2012, 153(4), 1875-1886.
[http://dx.doi.org/10.1210/en.2011-1975] [PMID: 22374971]
[62]
Lan, X.; Lu, G.; Yuan, C.; Mao, S.; Jiang, W.; Chen, Y.; Jin, X.; Xia, Q. Valproic acid (VPA) inhibits the epithelial-mesenchymal transition in prostate carcinoma via the dual suppression of SMAD4. J. Cancer Res. Clin. Oncol., 2016, 142(1), 177-185.
[http://dx.doi.org/10.1007/s00432-015-2020-4] [PMID: 26206483]
[63]
Zhang, H.; Wu, J.; Keller, J.M.; Yeung, K.; Keller, E.T.; Fu, Z. Transcriptional regulation of RKIP expression by androgen in prostate cells. Cell. Physiol. Biochem., 2012, 30(6), 1340-1350.
[http://dx.doi.org/10.1159/000343323] [PMID: 23095933]
[64]
Syed, V.; Mukherjee, K.; Lyons-Weiler, J.; Lau, K.M.; Mashima, T.; Tsuruo, T.; Ho, S.M. Identification of ATF-3, caveolin-1, DLC-1, and NM23-H2 as putative antitumorigenic, progesterone-regulated genes for ovarian cancer cells by gene profiling. Oncogene, 2005, 24(10), 1774-1787.
[http://dx.doi.org/10.1038/sj.onc.1207991] [PMID: 15674352]
[65]
Oppolzer, W.; Pimm, A.; Stammen, B.; Hume, W.E. Palladium-catalysed intramolecular cyclisations of olefinic propargylic carbonates and application to the diastereoselective synthesis of enantiomerically pure (-)-α-thujone. Helv. Chim. Acta, 1997, 80(3), 623-639.
[http://dx.doi.org/10.1002/hlca.19970800302]
[66]
Deiml, T.; Haseneder, R.; Zieglgänsberger, W.; Rammes, G.; Eisensamer, B.; Rupprecht, R.; Hapfelmeier, G. α-thujone reduces 5-HT3 receptor activity by an effect on the agonist-reduced desensitization. Neuropharmacology, 2004, 46(2), 192-201.
[http://dx.doi.org/10.1016/j.neuropharm.2003.09.022] [PMID: 15002407]
[67]
Liu, L.; Yang, C.; Shen, J.; Huang, L.; Lin, W.; Tang, H.; Liang, W.; Shao, W.; Zhang, H.; He, J. GABRA3 promotes lymphatic metastasis in lung adenocarcinoma by mediating upregulation of matrix metalloproteinases. Oncotarget, 2016, 7(22), 32341-32350.
[http://dx.doi.org/10.18632/oncotarget.8700] [PMID: 27081042]
[68]
Sizemore, G.M.; Sizemore, S.T.; Seachrist, D.D.; Keri, R.A. GABA(A) receptor pi (GABRP) stimulates basal-like breast cancer cell migration through activation of extracellular-regulated kinase 1/2 (ERK1/2). J. Biol. Chem., 2014, 289(35), 24102-24113.
[http://dx.doi.org/10.1074/jbc.M114.593582] [PMID: 25012653]
[69]
Neman, J.; Termini, J.; Wilczynski, S.; Vaidehi, N.; Choy, C.; Kowolik, C.M.; Li, H.; Hambrecht, A.C.; Roberts, E.; Jandial, R. Human breast cancer metastases to the brain display GABAergic properties in the neural niche. Proc. Natl. Acad. Sci. USA, 2014, 111(3), 984-989.
[http://dx.doi.org/10.1073/pnas.1322098111] [PMID: 24395782]
[70]
Siveen, K.S.; Kuttan, G. Thujone inhibits lung metastasis induced by B16F-10 melanoma cells in C57BL/6 mice. Can. J. Physiol. Pharmacol., 2011, 89(10), 691-703.
[http://dx.doi.org/10.1139/y11-067] [PMID: 21905822]
[71]
Patel, S.A.; Vanharanta, S. Epigenetic determinants of metastasis. Mol. Oncol., 2017, 11(1), 79-96.
[http://dx.doi.org/10.1016/j.molonc.2016.09.008] [PMID: 27756687]
[72]
Holm, K.; Grabau, D.; Lövgren, K.; Aradottir, S.; Gruvberger-Saal, S.; Howlin, J.; Saal, L.H.; Ethier, S.P.; Bendahl, P.O.; Stål, O.; Malmström, P.; Fernö, M.; Rydén, L.; Hegardt, C.; Borg, Å.; Ringnér, M. Global H3K27 trimethylation and EZH2 abundance in breast tumor subtypes. Mol. Oncol., 2012, 6(5), 494-506.
[http://dx.doi.org/10.1016/j.molonc.2012.06.002] [PMID: 22766277]
[73]
Varambally, S.; Dhanasekaran, S.M.; Zhou, M.; Barrette, T.R.; Kumar-Sinha, C.; Sanda, M.G.; Ghosh, D.; Pienta, K.J.; Sewalt, R.G.; Otte, A.P.; Rubin, M.A.; Chinnaiyan, A.M. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature, 2002, 419(6907), 624-629.
[http://dx.doi.org/10.1038/nature01075] [PMID: 12374981]
[74]
Gao, S.B.; Zheng, Q.F.; Xu, B.; Pan, C.B.; Li, K.L.; Zhao, Y.; Zheng, Q.L.; Lin, X.; Xue, L.X.; Jin, G.H. EZH2 represses target genes through H3K27-dependent and H3K27-independent mechanisms in hepatocellular carcinoma. Mol. Cancer Res., 2014, 12(10), 1388-1397.
[http://dx.doi.org/10.1158/1541-7786.MCR-14-0034] [PMID: 24916103]
[75]
Xu, C.; Hou, Z.; Zhan, P.; Zhao, W.; Chang, C.; Zou, J.; Hu, H.; Zhang, Y.; Yao, X.; Yu, L.; Yan, J. EZH2 regulates cancer cell migration through repressing TIMP-3 in non-small cell lung cancer. Med. Oncol., 2013, 30(4), 713.
[http://dx.doi.org/10.1007/s12032-013-0713-6] [PMID: 24132606]
[76]
Au, S.L.; Wong, C.C.; Lee, J.M.; Wong, C.M.; Ng, I.O. EZH2-mediated H3K27me3 is involved in epigenetic repression of deleted in liver cancer 1 in human cancers. PLoS One, 2013, 8(6) e68226
[http://dx.doi.org/10.1371/journal.pone.0068226] [PMID: 23826380]
[77]
Cao, Q.; Yu, J.; Dhanasekaran, S.M.; Kim, J.H.; Mani, R.S.; Tomlins, S.A.; Mehra, R.; Laxman, B.; Cao, X.; Yu, J.; Kleer, C.G.; Varambally, S.; Chinnaiyan, A.M. Repression of E-cadherin by the polycomb group protein EZH2 in cancer. Oncogene, 2008, 27(58), 7274-7284.
[http://dx.doi.org/10.1038/onc.2008.333] [PMID: 18806826]
[78]
Kantarjian, H.; Issa, J.P.; Rosenfeld, C.S.; Bennett, J.M.; Albitar, M.; DiPersio, J.; Klimek, V.; Slack, J.; de Castro, C.; Ravandi, F.; Helmer, R., III; Shen, L.; Nimer, S.D.; Leavitt, R.; Raza, A.; Saba, H. Decitabine improves patient outcomes in myelodysplastic syndromes: results of a phase III randomized study. Cancer, 2006, 106(8), 1794-1803.
[http://dx.doi.org/10.1002/cncr.21792] [PMID: 16532500]
[79]
Christman, J.K.; Mendelsohn, N.; Herzog, D.; Schneiderman, N. Effect of 5-azacytidine on differentiation and DNA methylation in human promyelocytic leukemia cells (HL-60). Cancer Res., 1983, 43(2), 763-769.
[PMID: 6184156]
[80]
Hartsough, M.T.; Clare, S.E. Mair, Michael.; Elkahloun, A.G.; Sgroi, D.; Osborne, K. Elevation of breast carcinoma Nm23-H1 metastasis suppressor gene expression and reduced mobility by DNA methylation inhibition. Cancer Res., 2001, 61, 2320-2327.
[PMID: 11280805]
[81]
Chang, X.; Zhang, S.; Ma, J.; Li, Z.; Zhi, Y.; Chen, J.; Lu, Y.; Dai, D. Association of NDRG1 gene promoter methylation with reduced NDRG1 expression in gastric cancer cells and tissue specimens. Cell Biochem. Biophys., 2013, 66(1), 93-101.
[http://dx.doi.org/10.1007/s12013-012-9457-8] [PMID: 23099645]
[82]
Bandyopadhyay, S.; Pai, S.K.; Hirota, S.; Hosobe, S.; Takano, Y.; Saito, K.; Piquemal, D.; Commes, T.; Watabe, M.; Gross, S.C.; Wang, Y.; Ran, S.; Watabe, K. Role of the putative tumor metastasis suppressor gene Drg-1 in breast cancer progression. Oncogene, 2004, 23(33), 5675-5681.
[http://dx.doi.org/10.1038/sj.onc.1207734] [PMID: 15184886]
[83]
Metge, B.J.; Frost, A.R.; King, J.A.; Dyess, D.L.; Welch, D.R.; Samant, R.S.; Shevde, L.A. Epigenetic silencing contributes to the loss of BRMS1 expression in breast cancer. Clin. Exp. Metastasis, 2008, 25(7), 753-763.
[http://dx.doi.org/10.1007/s10585-008-9187-x] [PMID: 18566899]
[84]
Arab, K.; Smith, L.T.; Gast, A.; Weichenhan, D.; Huang, J.P.; Claus, R.; Hielscher, T.; Espinosa, A.V.; Ringel, M.D.; Morrison, C.D.; Schadendorf, D.; Kumar, R.; Plass, C. Epigenetic deregulation of TCF21 inhibits metastasis suppressor KISS1 in metastatic melanoma. Carcinogenesis, 2011, 32(10), 1467-1473.
[http://dx.doi.org/10.1093/carcin/bgr138] [PMID: 21771727]
[85]
Hull, E.E.; Montgomery, M.R.; Leyva, K.J. HDAC inhibitors as epigenetic regulators of the immune system: Impacts on cancer therapy and inflammatory diseases. BioMed Res. Int., 2016, 2016 8797206
[http://dx.doi.org/10.1155/2016/8797206] [PMID: 27556043]
[86]
Kakihana, M.; Ohira, T.; Chan, D.; Webster, R.B.; Kato, H.; Drabkin, H.A.; Gemmill, R.M. Induction of E-cadherin in lung cancer and interaction with growth suppression by histone deacetylase inhibition. J. Thorac. Oncol., 2009, 4(12), 1455-1465.
[http://dx.doi.org/10.1097/JTO.0b013e3181bc9419] [PMID: 20009910]
[87]
Catalano, M.G.; Fortunati, N.; Pugliese, M.; Marano, F.; Ortoleva, L.; Poli, R.; Asioli, S.; Bandino, A.; Palestini, N.; Grange, C.; Bussolati, B.; Boccuzzi, G. Histone deacetylase inhibition modulates E-cadherin expression and suppresses migration and invasion of anaplastic thyroid cancer cells. J. Clin. Endocrinol. Metab., 2012, 97(7), E1150-E1159.
[http://dx.doi.org/10.1210/jc.2011-2970] [PMID: 22563106]
[88]
Joseph, J.; Mudduluru, G.; Antony, S.; Vashistha, S.; Ajitkumar, P.; Somasundaram, K. Expression profiling of sodium butyrate (NaB)-treated cells: identification of regulation of genes related to cytokine signaling and cancer metastasis by NaB. Oncogene, 2004, 23(37), 6304-6315.
[http://dx.doi.org/10.1038/sj.onc.1207852] [PMID: 15318170]
[89]
Meehan, W.J.; Samant, R.S.; Hopper, J.E.; Carrozza, M.J.; Shevde, L.A.; Workman, J.L.; Eckert, K.A.; Verderame, M.F.; Welch, D.R. Breast cancer metastasis suppressor 1 (BRMS1) forms complexes with retinoblastoma-binding protein 1 (RBP1) and the mSin3 histone deacetylase complex and represses transcription. J. Biol. Chem., 2004, 279(2), 1562-1569.
[http://dx.doi.org/10.1074/jbc.M307969200] [PMID: 14581478]
[90]
Cicek, M.; Fukuyama, R.; Cicek, M.S.; Sizemore, S.; Welch, D.R.; Sizemore, N.; Casey, G. BRMS1 contributes to the negative regulation of uPA gene expression through recruitment of HDAC1 to the NF-kappaB binding site of the uPA promoter. Clin. Exp. Metastasis, 2009, 26(3), 229-237.
[http://dx.doi.org/10.1007/s10585-009-9235-1] [PMID: 19165610]
[91]
Samant, R.S.; Seraj, M.J.; Saunders, M.M.; Sakamaki, T.S.; Shevde, L.A.; Harms, J.F.; Leonard, T.O.; Goldberg, S.F.; Budgeon, L.; Meehan, W.J.; Winter, C.R.; Christensen, N.D.; Verderame, M.F.; Donahue, H.J.; Welch, D.R. Analysis of mechanisms underlying BRMS1 suppression of metastasis. Clin. Exp. Metastasis, 2000, 18(8), 683-693.
[http://dx.doi.org/10.1023/A:1013124725690] [PMID: 11827072]
[92]
Angst, E.; Dawson, D.W.; Nguyen, A.; Park, J.; Go, V.L.W.; Reber, H.A.; Hines, O.J.; Eibl, G. Epigenetic regulation affects N-myc downstream-regulated gene 1 expression indirectly in pancreatic cancer cells. Pancreas, 2010, 39(5), 675-679.
[http://dx.doi.org/10.1097/MPA.0b013e3181c8b476] [PMID: 20173668]
[93]
Nebbioso, A.; Carafa, V.; Benedetti, R.; Altucci, L. Trials with ‘epigenetic’ drugs: an update. Mol. Oncol., 2012, 6(6), 657-682.
[http://dx.doi.org/10.1016/j.molonc.2012.09.004] [PMID: 23103179]
[94]
Liao, C.H.; Sang, S.; Ho, C.T.; Lin, J.K. Garcinol modulates tyrosine phosphorylation of FAK and subsequently induces apoptosis through down-regulation of Src, ERK, and Akt survival signaling in human colon cancer cells. J. Cell. Biochem., 2005, 96(1), 155-169.
[http://dx.doi.org/10.1002/jcb.20540] [PMID: 16052481]
[95]
Chatterjee, D.; Bai, Y.; Wang, Z.; Beach, S.; Mott, S.; Roy, R.; Braastad, C.; Sun, Y.; Mukhopadhyay, A.; Aggarwal, B.B.; Darnowski, J.; Pantazis, P.; Wyche, J.; Fu, Z.; Kitagwa, Y.; Keller, E.T.; Sedivy, J.M.; Yeung, K.C. RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis. J. Biol. Chem., 2004, 279(17), 17515-17523.
[http://dx.doi.org/10.1074/jbc.M313816200] [PMID: 14766752]
[96]
Volk-Draper, L.; Hall, K.; Griggs, C.; Rajput, S.; Kohio, P.; DeNardo, D.; Ran, S. Paclitaxel therapy promotes breast cancer metastasis in a TLR4-dependent manner. Cancer Res., 2014, 74(19), 5421-5434.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-0067] [PMID: 25274031]
[97]
Li, Q.; Ma, Z.; Liu, Y.; Kan, X.; Wang, C.; Su, B.; Li, Y.; Zhang, Y.; Wang, P.; Luo, Y.; Na, D.; Wang, L.; Zhang, G.; Zhu, X.; Wang, L. Low doses of paclitaxel enhance liver metastasis of breast cancer cells in the mouse model. FEBS J., 2016, 283(15), 2836-2852.
[http://dx.doi.org/10.1111/febs.13767] [PMID: 27307301]
[98]
Piskounova, E.; Agathocleous, M.; Murphy, M.M.; Hu, Z.; Huddlestun, S.E.; Zhao, Z.; Leitch, A.M.; Johnson, T.M.; DeBerardinis, R.J.; Morrison, S.J. Oxidative stress inhibits distant metastasis by human melanoma cells. Nature, 2015, 527(7577), 186-191.
[http://dx.doi.org/10.1038/nature15726] [PMID: 26466563]
[99]
Park, S.; Ahn, E.S.; Lee, S.; Jung, M.; Park, J.H.; Yi, S.Y.; Yeom, C.H. Proteomic analysis reveals upregulation of RKIP in S-180 implanted BALB/C mouse after treatment with ascorbic acid. J. Cell. Biochem., 2009, 106(6), 1136-1145.
[http://dx.doi.org/10.1002/jcb.22097] [PMID: 19224539]
[100]
Singhal, J.; Nagaprashantha, L.D.; Vatsyayan, R. Ashutosh; Awasthi, S.; Singhal, S.S. Didymin induces apoptosis by inhibiting N-Myc and upregulating RKIP in neuroblastoma. Cancer Prev. Res. (Phila.), 2012, 5(3), 473-483.
[http://dx.doi.org/10.1158/1940-6207.CAPR-11-0318] [PMID: 22174364]
[101]
Wei, J.; Huang, Q.; Bai, F.; Lin, J.; Nie, J.; Lu, S.; Lu, C.; Huang, R.; Lu, Z.; Lin, X. Didymin induces apoptosis through mitochondrial dysfunction and up-regulation of RKIP in human hepatoma cells. Chem. Biol. Interact., 2017, 261, 118-126.
[http://dx.doi.org/10.1016/j.cbi.2016.11.026] [PMID: 27899290]
[102]
Kim, S.O.; Kim, M.R. (-)-Epigallocatechin 3-gallate inhibits invasion by inducing the expression of Raf kinase inhibitor protein in AsPC1 human pancreatic adenocarcinoma cells through the modulation of histone deacetylase activity. Int. J. Oncol., 2013, 42(1), 349-358.
[http://dx.doi.org/10.3892/ijo.2012.1686] [PMID: 23135610]
[103]
Keshmiri-Neghab, H.; Goliaei, B. Therapeutic potential of gossypol: an overview. Pharm. Biol., 2014, 52(1), 124-128.
[http://dx.doi.org/10.3109/13880209.2013.832776] [PMID: 24073600]
[104]
Huang, Y.W.; Wang, L.S.; Dowd, M.K.; Wan, P.J.; Lin, Y.C. (-)-Gossypol reduces invasiveness in metastatic prostate cancer cells. Anticancer Res., 2009, 29(6), 2179-2188.
[PMID: 19528479]
[105]
Ono, M.; Takeshima, M.; Nakano, S. Mechanism of the anticancer effect of lycopene (tetraterpenoids). Enzymes, 2015, 37, 139-166.
[http://dx.doi.org/10.1016/bs.enz.2015.06.002] [PMID: 26298459]
[106]
Palozza, P.; Parrone, N.; Catalano, A.; Simone, R. Tomato lycopene and inflammatory cascade: basic interactions and clinical implications. Curr. Med. Chem., 2010, 17(23), 2547-2563.
[http://dx.doi.org/10.2174/092986710791556041] [PMID: 20491642]
[107]
Huang, C.S.; Shih, M.K.; Chuang, C.H.; Hu, M.L. Lycopene inhibits cell migration and invasion and upregulates Nm23-H1 in a highly invasive hepatocarcinoma, SK-Hep-1 cells. J. Nutr., 2005, 135(9), 2119-2123.
[http://dx.doi.org/10.1093/jn/135.9.2119] [PMID: 16140886]
[108]
Ji, Q.; Zheng, G.Y.; Xia, W.; Chen, J.Y.; Meng, X.Y.; Zhang, H.; Rahman, K.; Xin, H.L. Inhibition of invasion and metastasis of human liver cancer HCCLM3 cells by portulacerebroside A. Pharm. Biol., 2015, 53(5), 773-780.
[http://dx.doi.org/10.3109/13880209.2014.941505] [PMID: 25472720]
[109]
Ye, Q.; Liao, X.; Fu, P.; Dou, J.; Chen, K.; Jiang, H. Portulacerebroside A inhibits adhesion, migration, and invasion of human leukemia HL60 cells and U937 cells through the regulation of p38/JNK signaling pathway. OncoTargets Ther., 2016, 9, 6953-6963.
[http://dx.doi.org/10.2147/OTT.S117523] [PMID: 27956839]
[110]
Heyninck, K.; Lahtela-Kakkonen, M.; Van der Veken, P.; Haegeman, G.; Vanden Berghe, W. Withaferin A inhibits NF-kappaB activation by targeting cysteine 179 in IKKβ. Biochem. Pharmacol., 2014, 91(4), 501-509.
[http://dx.doi.org/10.1016/j.bcp.2014.08.004] [PMID: 25159986]
[111]
Szarc vel Szic, K.; Op de Beeck, K.; Ratman, D.; Wouters, A.; Beck, I.M.; Declerck, K.; Heyninck, K.; Fransen, E.; Bracke, M.; De Bosscher, K.; Lardon, F.; Van Camp, G.; Vanden Berghe, W. Pharmacological levels of Withaferin A (Withania somnifera) trigger clinically relevant anticancer effects specific to triple negative breast cancer cells. PLoS One, 2014, 9(2)e87850
[http://dx.doi.org/10.1371/journal.pone.0087850] [PMID: 24498382]
[112]
Bargagna-Mohan, P.; Hamza, A.; Kim, Y.E.; Khuan Abby Ho, Y.; Mor-Vaknin, N.; Wendschlag, N.; Liu, J.; Evans, R.M.; Markovitz, D.M.; Zhan, C.G.; Kim, K.B.; Mohan, R. The tumor inhibitor and antiangiogenic agent withaferin A targets the intermediate filament protein vimentin. Chem. Biol., 2007, 14(6), 623-634.
[http://dx.doi.org/10.1016/j.chembiol.2007.04.010] [PMID: 17584610]
[113]
Hsu, Y.L.; Chen, C.Y.; Lin, I.P.; Tsai, E.M.; Kuo, P.L.; Hou, M.F. 4-Shogaol, an active constituent of dietary ginger, inhibits metastasis of MDA-MB-231 human breast adenocarcinoma cells by decreasing the repression of NF-κB/Snail on RKIP. J. Agric. Food Chem., 2012, 60(3), 852-861.
[http://dx.doi.org/10.1021/jf2052515] [PMID: 22224671]
[114]
Chaudhary, L.R.; Hruska, K.A. Inhibition of cell survival signal protein kinase B/Akt by curcumin in human prostate cancer cells. J. Cell. Biochem., 2003, 89(1), 1-5.
[http://dx.doi.org/10.1002/jcb.10495] [PMID: 12682902]
[115]
Wang, Z.; Zhang, Y.; Banerjee, S.; Li, Y.; Sarkar, F.H. Notch-1 down-regulation by curcumin is associated with the inhibition of cell growth and the induction of apoptosis in pancreatic cancer cells. Cancer, 2006, 106(11), 2503-2513.
[http://dx.doi.org/10.1002/cncr.21904] [PMID: 16628653]
[116]
Zhang, F.; Zhang, Z.; Chen, L.; Kong, D.; Zhang, X.; Lu, C.; Lu, Y.; Zheng, S. Curcumin attenuates angiogenesis in liver fibrosis and inhibits angiogenic properties of hepatic stellate cells. J. Cell. Mol. Med., 2014, 18(7), 1392-1406.
[http://dx.doi.org/10.1111/jcmm.12286] [PMID: 24779927]
[117]
Bachmeier, B.; Nerlich, A.G.; Iancu, C.M.; Cilli, M.; Schleicher, E.; Vené, R.; Dell’Eva, R.; Jochum, M.; Albini, A.; Pfeffer, U. The chemopreventive polyphenol Curcumin prevents hematogenous breast cancer metastases in immunodeficient mice. Cell. Physiol. Biochem., 2007, 19(1-4), 137-152.
[http://dx.doi.org/10.1159/000099202] [PMID: 17310108]
[118]
Chen, C.C.; Sureshbabul, M.; Chen, H.W.; Lin, Y.S.; Lee, J.Y.; Hong, Q.S.; Yang, Y.C.; Yu, S.L. Curcumin suppresses metastasis via Sp-1, FAK inhibition, and E-cadherin upregulation in colorectal cancer. Evid. Based Complement. Alternat. Med., 2013, 2013 541695
[http://dx.doi.org/10.1155/2013/541695] [PMID: 23970932]
[119]
Mukherjee, S.; Mazumdar, M.; Chakraborty, S.; Manna, A.; Saha, S.; Khan, P.; Bhattacharjee, P.; Guha, D.; Adhikary, A.; Mukhjerjee, S.; Das, T. Curcumin inhibits breast cancer stem cell migration by amplifying the E-cadherin/β-catenin negative feedback loop. Stem Cell Res. Ther., 2014, 5(5), 116.
[http://dx.doi.org/10.1186/scrt506] [PMID: 25315241]
[120]
Guo, Y.; Shu, L.; Zhang, C.; Su, Z.Y.; Kong, A.N.T. Curcumin inhibits anchorage-independent growth of HT29 human colon cancer cells by targeting epigenetic restoration of the tumor suppressor gene DLEC1. Biochem. Pharmacol., 2015, 94(2), 69-78.
[http://dx.doi.org/10.1016/j.bcp.2015.01.009] [PMID: 25640947]
[121]
Liu, Y.; Zhou, J.; Hu, Y.; Wang, J.; Yuan, C. Curcumin inhibits growth of human breast cancer cells through demethylation of DLC1 promoter. Mol. Cell. Biochem., 2017, 425(1-2), 47-58.
[http://dx.doi.org/10.1007/s11010-016-2861-4] [PMID: 27830358]
[122]
Tahara, E.; Kadara, H.; Lacroix, L.; Lotan, D.; Lotan, R. Activation of protein kinase C by phorbol 12-myristate 13-acetate suppresses the growth of lung cancer cells through KLF6 induction. Cancer Biol. Ther., 2009, 8(9), 801-807.
[http://dx.doi.org/10.4161/cbt.8.9.8186] [PMID: 19333010]
[123]
Fortino, V.; Torricelli, C.; Capurro, E.; Sacchi, G.; Valacchi, G.; Maioli, E. Antiproliferative and survival properties of PMA in MCF-7 breast cancer cell. Cancer Invest., 2008, 26(1), 13-21.
[http://dx.doi.org/10.1080/07357900701637949] [PMID: 18181040]
[124]
Rowe, A.; Weiske, J.; Kramer, T.S.; Huber, O.; Jackson, P. Phorbol ester enhances KAI1 transcription by recruiting Tip60/Pontin complexes. Neoplasia, 2008, 10(12), 1421-1432, 1432.
[http://dx.doi.org/10.1593/neo.08850] [PMID: 19048121]
[125]
Le, N.T.; Richardson, D.R. Iron chelators with high antiproliferative activity up-regulate the expression of a growth inhibitory and metastasis suppressor gene: a link between iron metabolism and proliferation. Blood, 2004, 104(9), 2967-2975.
[http://dx.doi.org/10.1182/blood-2004-05-1866] [PMID: 15251988]
[126]
Chung, L.C.; Tsui, K.H.; Feng, T.H.; Lee, S.L.; Chang, P.L.; Juang, H.H. L-Mimosine blocks cell proliferation via upregulation of B-cell translocation gene 2 and N-myc downstream regulated gene 1 in prostate carcinoma cells. Am. J. Physiol. Cell Physiol., 2012, 302(4), C676-C685.
[http://dx.doi.org/10.1152/ajpcell.00180.2011] [PMID: 22116304]
[127]
Chen, Z.; Zhang, D.; Yue, F.; Zheng, M.; Kovacevic, Z.; Richardson, D.R. The iron chelators Dp44mT and DFO inhibit TGF-β-induced epithelial-mesenchymal transition via up-regulation of N-Myc downstream-regulated gene 1 (NDRG1). J. Biol. Chem., 2012, 287(21), 17016-17028.
[http://dx.doi.org/10.1074/jbc.M112.350470] [PMID: 22453918]
[128]
Angst, E.; Sibold, S.; Tiffon, C.; Weimann, R.; Gloor, B.; Candinas, D.; Stroka, D. Cellular differentiation determines the expression of the hypoxia-inducible protein NDRG1 in pancreatic cancer. Br. J. Cancer, 2006, 95(3), 307-313.
[http://dx.doi.org/10.1038/sj.bjc.6603256] [PMID: 16832411]
[129]
Cummins, E.P.; Berra, E.; Comerford, K.M.; Ginouves, A.; Fitzgerald, K.T.; Seeballuck, F.; Godson, C.; Nielsen, J.E.; Moynagh, P.; Pouyssegur, J.; Taylor, C.T. Prolyl hydroxylase-1 negatively regulates IkappaB kinase-β, giving insight into hypoxia-induced NFkappaB activity. Proc. Natl. Acad. Sci. USA, 2006, 103(48), 18154-18159.
[http://dx.doi.org/10.1073/pnas.0602235103] [PMID: 17114296]
[130]
Sibold, S.; Roh, V.; Keogh, A.; Studer, P.; Tiffon, C.; Angst, E.; Vorburger, S.A.; Weimann, R.; Candinas, D.; Stroka, D. Hypoxia increases cytoplasmic expression of NDRG1, but is insufficient for its membrane localization in human hepatocellular carcinoma. FEBS Lett., 2007, 581(5), 989-994.
[http://dx.doi.org/10.1016/j.febslet.2007.01.080] [PMID: 17316623]
[131]
Davidson, T.; Salnikow, K.; Costa, M. Hypoxia inducible factor-1 α-independent suppression of aryl hydrocarbon receptor-regulated genes by nickel. Mol. Pharmacol., 2003, 64(6), 1485-1493.
[http://dx.doi.org/10.1124/mol.64.6.1485] [PMID: 14645679]
[132]
An, X.; Tiwari, A.K.; Sun, Y.; Ding, P.R.; Ashby, C.R., Jr; Chen, Z.S. BCR-ABL tyrosine kinase inhibitors in the treatment of Philadelphia chromosome positive chronic myeloid leukemia: a review. Leuk. Res., 2010, 34(10), 1255-1268.
[http://dx.doi.org/10.1016/j.leukres.2010.04.016] [PMID: 20537386]
[133]
Mirshafiey, A.; Ghalamfarsa, G.; Asghari, B.; Azizi, G. Receptor tyrosine kinase and tyrosine kinase inhibitors: new hope for success in multiple sclerosis therapy. Innov. Clin. Neurosci., 2014, 11(7-8), 23-36.
[PMID: 25337443]
[134]
Fernandes, B.F.; Di Cesare, S.; Neto Belfort, R.; Maloney, S.; Martins, C.; Castiglione, E.; Isenberg, J.; Abourbih, D.; Antecka, E.; Burnier, M.N., Jr Imatinib mesylate alters the expression of genes related to disease progression in an animal model of uveal melanoma. Anal. Cell. Pathol. (Amst.), 2011, 34(3), 123-130.
[http://dx.doi.org/10.1155/2011/210816] [PMID: 21606571]
[135]
Keshavarz-Pakseresht, B.; Shandiz, S.A.S.; Baghbani-Arani, F. Imatinib induces up-regulation of NM23, a metastasis suppressor gene, in human Hepatocarcinoma (HepG2) Cell Line. Gastroenterol. Hepatol. Bed Bench, 2017, 10(1), 29-33.
[PMID: 28331561]
[136]
Shandiz, S.A.S.; Khosravani, M.; Mohammadi, S.; Noorbazargan, H.; Mirzaie, A.; Inanlou, D.N.; Dalirsaber, M.D.; Jouzaghkar, H.; Baghbani-Arani, F.; Keshavarz-Pakseresht, B. Evaluation of imatinib mesylate (Gleevec) on gene expression in breast cancer MCF-7 cells using quantitative real-time PCR. Asian Pac. J. Trop. Biomed., 2016, 6, 159-163.
[http://dx.doi.org/10.1016/j.apjtb.2015.10.006]
[137]
Berridge, M.J.; Lipp, P.; Bootman, M.D. Signal transduction. The calcium entry pas de deux. Science, 2000, 287(5458), 1604-1605.
[http://dx.doi.org/10.1126/science.287.5458.1604] [PMID: 10733429]
[138]
Zhang, C.; Lv, F.; Zhou, L.; Li, X.; Wu, X.X.; Hoffman, R.M. Effect of verapamil on the expression of EGFR and NM23 in A549 human lung cancer cells. Anticancer Res., 2009, 29(1), 27-32.
[PMID: 19331130]
[139]
Siddikuzzaman; Guruvayoorappan, C.; Berlin Grace, V.M. All trans retinoic acid and cancer. Immunopharmacol. Immunotoxicol., 2011, 33(2), 241-249.
[http://dx.doi.org/10.3109/08923973.2010.521507] [PMID: 20929432]
[140]
Liu, F.; Qi, H.L.; Chen, H.L. Effects of all-trans retinoic acid and epidermal growth factor on the expression of nm23-H1 in human hepatocarcinoma cells. J. Cancer Res. Clin. Oncol., 2000, 126(2), 85-90.
[PMID: 10664247]
[141]
Lilly, A.J.; Khanim, F.L.; Bunce, C.M. The case for extracellular Nm23-H1 as a driver of Acute Myeloid Leukaemia (AML) progression. Naunyn Schmiedebergs Arch. Pharmacol., 2015, 388(2), 225-233.
[http://dx.doi.org/10.1007/s00210-014-1027-8] [PMID: 25119778]
[142]
Singh, N.P.; Lai, H. Selective toxicity of dihydroartemisinin and holotransferrin toward human breast cancer cells. Life Sci., 2001, 70(1), 49-56.
[http://dx.doi.org/10.1016/S0024-3205(01)01372-8] [PMID: 11764006]
[143]
Chen, T.; Li, M.; Zhang, R.; Wang, H. Dihydroartemisinin induces apoptosis and sensitizes human ovarian cancer cells to carboplatin therapy. J. Cell. Mol. Med., 2009, 13(7), 1358-1370.
[http://dx.doi.org/10.1111/j.1582-4934.2008.00360.x] [PMID: 18466355]
[144]
Hu, C.J.; Zhou, L.; Cai, Y. Dihydroartemisinin induces apoptosis of cervical cancer cells via upregulation of RKIP and downregulation of bcl-2. Cancer Biol. Ther., 2014, 15(3), 279-288.
[http://dx.doi.org/10.4161/cbt.27223] [PMID: 24335512]
[145]
Ogino, H.; Fujii, M.; Ono, M.; Maezawa, K.; Hori, S.; Kizu, J. In vivo and in vitro effects of fluoroquinolones on lipopolysaccharide-induced pro-inflammatory cytokine production. J. Infect. Chemother., 2009, 15(3), 168-173.
[http://dx.doi.org/10.1007/s10156-009-0680-1] [PMID: 19554401]
[146]
Kan, J.Y.; Hsu, Y.L.; Chen, Y.H.; Chen, T.C.; Wang, J.Y.; Kuo, P.L. Gemifloxacin, a fluoroquinolone antimicrobial drug, inhibits migration and invasion of human colon cancer cells. BioMed Res. Int., 2013, 2013 159786
[http://dx.doi.org/10.1155/2013/159786] [PMID: 24386633]
[147]
Li, X.M.; Jia, L.F.; Lu, X.Y.; Shen, Y.P.; Li, Z.; Song, Q. Dihydroartemisinin is a newly defined STAT3 inhibitor that may be of multiple potential uses in cancer treatment. Cancer Cell Microenviron., 2016, 3(2) e1254
[148]
Yang, Y.; Park, S.Y.; Nguyen, T.T.; Yu, Y.H.; Nguyen, T.V.; Sun, E.G.; Udeni, J.; Jeong, M.H.; Pereira, I.; Moon, C.; Ha, H.H.; Kim, K.K.; Hur, J.S.; Kim, H. Lichen secondary metabolite, physciosporin, inhibits lung cancer cell motility. PLoS One, 2015, 10(9) e0137889
[http://dx.doi.org/10.1371/journal.pone.0137889] [PMID: 26371759]
[149]
Stelzer, G.; Rosen, N.; Plaschkes, I.; Zimmerman, S.; Twik, M.; Fishilevich, S.; Stein, T.I.; Nudel, R.; Lieder, I.; Mazor, Y.; Kaplan, S. The GeneCards suite: from gene data mining to disease genome sequence analyses. Curr. Protoc. Bioinformatics, 2016, 54(1), 1-30.
[http://dx.doi.org/10.1002/cpbi.5] [PMID: 27322403]
[150]
Arinze, I.J.; Kawai, Y. Sp family of transcription factors is involved in valproic acid-induced expression of Galphai2. J. Biol. Chem., 2003, 278(20), 17785-17791.
[http://dx.doi.org/10.1074/jbc.M209430200] [PMID: 12624107]
[151]
Tso, P.H.; Wang, Y.; Yung, L.Y.; Tong, Y.; Lee, M.M.K.; Wong, Y.H. RGS19 inhibits Ras signaling through Nm23H1/2-mediated phosphorylation of the kinase suppressor of Ras. Cell. Signal., 2013, 25(5), 1064-1074.
[http://dx.doi.org/10.1016/j.cellsig.2013.02.010] [PMID: 23416464]
[152]
Wang, Y.; Tong, Y.; Tso, P.H.; Wong, Y.H. Regulator of G protein signaling 19 suppresses Ras-induced neoplastic transformation and tumorigenesis. Cancer Lett., 2013, 339(1), 33-41.
[http://dx.doi.org/10.1016/j.canlet.2013.07.025] [PMID: 23911936]
[153]
Song, W.J.; Mondal, P.; Wolfe, A.; Alonso, L.C.; Stamateris, R.; Ong, B.W.T.; Lim, O.C.; Yang, K.S.; Radovick, S.; Novaira, H.J.; Farber, E.A.; Farber, C.R.; Turner, S.D.; Hussain, M.A. Glucagon regulates hepatic kisspeptin to impair insulin secretion. Cell Metab., 2014, 19(4), 667-681.
[http://dx.doi.org/10.1016/j.cmet.2014.03.005] [PMID: 24703698]
[154]
Zhang, B.; Wang, O.; Qin, J.; Liu, S.; Sun, S.; Liu, H.; Kuang, J.; Jiang, G.; Zhang, W. cis-acting elements and trans-acting factors in the transcriptional regulation of raf kinase inhibitory protein expression. PLoS One, 2013, 8(12) e83097
[http://dx.doi.org/10.1371/journal.pone.0083097] [PMID: 24386147]
[155]
Yang, Y.L.; Chen, C.Z.; Jin, L.P.; Ji, Q.Q.; Chen, Y.Z.; Li, Q.; Zhang, X.H.; Qu, J.M. Effect and mechanism of the metastasis suppressor gene BRMS1 on the migration of breast cancer cells. Int. J. Clin. Exp. Med., 2013, 6(10), 908-916.
[PMID: 24260596]
[156]
Ko, F.C.F.; Chan, L.K.; Sze, K.M.; Yeung, Y.S.; Tse, E.Y.; Lu, P.; Yu, M.H.; Ng, I.O.L.; Yam, J.W.P. PKA-induced dimerization of the RhoGAP DLC1 promotes its inhibition of tumorigenesis and metastasis. Nat. Commun., 2013, 4, 1618.
[http://dx.doi.org/10.1038/ncomms2604] [PMID: 23511482]
[157]
Liu, W.; Iiizumi-Gairani, M.; Okuda, H.; Kobayashi, A.; Watabe, M.; Pai, S.K.; Pandey, P.R.; Xing, F.; Fukuda, K.; Modur, V.; Hirota, S.; Suzuki, K.; Chiba, T.; Endo, M.; Sugai, T.; Watabe, K. KAI1 gene is engaged in NDRG1 gene-mediated metastasis suppression through the ATF3-NFkappaB complex in human prostate cancer. J. Biol. Chem., 2011, 286(21), 18949-18959.
[http://dx.doi.org/10.1074/jbc.M111.232637] [PMID: 21454613]
[158]
Michael, L.F.; Asahara, H.; Shulman, A.I.; Kraus, W.L.; Montminy, M. The phosphorylation status of a cyclic AMP-responsive activator is modulated via a chromatin-dependent mechanism. Mol. Cell. Biol., 2000, 20(5), 1596-1603.
[http://dx.doi.org/10.1128/MCB.20.5.1596-1603.2000] [PMID: 10669737]
[159]
Fass, D.M.; Butler, J.E.F.; Goodman, R.H. Deacetylase activity is required for cAMP activation of a subset of CREB target genes. J. Biol. Chem., 2003, 278(44), 43014-43019.
[http://dx.doi.org/10.1074/jbc.M305905200] [PMID: 12939274]
[160]
Shen, H.Y.; Kalda, A.; Yu, L.; Ferrara, J.; Zhu, J.; Chen, J.F. Additive effects of histone deacetylase inhibitors and amphetamine on histone H4 acetylation, cAMP responsive element binding protein phosphorylation and DeltaFosB expression in the striatum and locomotor sensitization in mice. Neuroscience, 2008, 157(3), 644-655.
[http://dx.doi.org/10.1016/j.neuroscience.2008.09.019] [PMID: 18848971]
[161]
Miller, K.D.; Althouse, S.K.; Nabell, L.; Rugo, H.; Carey, L.; Kimmick, G.; Jones, D.R.; Merino, M.J.; Steeg, P.S. A phase II study of medroxyprogesterone acetate in patients with hormone receptor negative metastatic breast cancer: translational breast cancer research consortium trial 007. Breast Cancer Res. Treat., 2014, 148(1), 99-106.
[http://dx.doi.org/10.1007/s10549-014-3131-3] [PMID: 25257727]


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VOLUME: 26
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Year: 2019
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