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Current Cancer Drug Targets

Editor-in-Chief

ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

Research Article

Curcumin Inhibits Vasculogenic Mimicry via Regulating ETS-1 in Renal Cell Carcinoma

Author(s): Yue Chong, Shan Xu, Tianjie Liu, Peng Guo, Xinyang Wang, Dalin He* and Guodong Zhu*

Volume 24, Issue 10, 2024

Published on: 30 January, 2024

Page: [1031 - 1046] Pages: 16

DOI: 10.2174/0115680096277126240102060617

Price: $65

Abstract

Background: Metastatic renal cell carcinoma (RCC) poses a huge challenge once it has become resistant to targeted therapy. Vasculogenic mimicry (VM) is a novel blood supply system formed by tumor cells that can circumvent molecular targeted therapies. As one of the herbal remedies, curcumin has been demonstrated to play antineoplastic effects in many different types of human cancers; however, its function and mechanism of targeting VM in RCC remains unknown.

Objective: Here, in the work, we explored the role of curcumin and its molecular mechanism in the regulation of VM formation in RCC.

Methods: RNA-sequencing analysis, immunoblotting, and immunohistochemistry were used to detect E Twenty Six-1(ETS-1), vascular endothelial Cadherin (VE-Cadherin), and matrix metallopeptidase 9 (MMP9) expressions in RCC cells and tissues. RNA sequencing was used to screen the differential expressed genes. Plasmid transfections were used to transiently knock down or overexpress ETS-1. VM formation was determined by tube formation assay and animal experiments. CD31-PAS double staining was used to label the VM channels in patients and xenograft samples.

Results: Our results demonstrated that VM was positively correlated with RCC grades and stages using clinical patient samples. Curcumin inhibited VM formation in dose and time-dependent manner in vitro. Using RNA-sequencing analysis, we discovered ETS-1 as a potential transcriptional factor regulating VM formation. Knocking down or overexpression of ETS-1 decreased or increased the VM formation, respectively and regulated the expression of VE-Cadherin and MMP9. Curcumin could inhibit VM formation by suppressing ETS-1, VE-Cadherin, and MMP9 expression both in vitro and in vivo.

Conclusion: Our finding might indicate that curcumin could inhibit VM by regulating ETS-1, VE-Cadherin, and MMP9 expression in RCC cell lines. Curcumin could be considered as a potential anti-cancer compound by inhibiting VM in RCC progression.

Graphical Abstract

[1]
Rini, B.I.; Campbell, S.C.; Escudier, B. Renal cell carcinoma. Lancet, 2009, 373(9669), 1119-1132.
[http://dx.doi.org/10.1016/S0140-6736(09)60229-4] [PMID: 19269025]
[2]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 Countries. CA Cancer J. Clin., 2021, 71(3), 209-249.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[3]
Moch, H.; Cubilla, A.L.; Humphrey, P.A.; Reuter, V.E.; Ulbright, T.M. The 2016 WHO classification of tumours of the urinary system and male genital organs—part A: Renal, penile, and testicular tumours. Eur. Urol., 2016, 70(1), 93-105.
[http://dx.doi.org/10.1016/j.eururo.2016.02.029] [PMID: 26935559]
[4]
Wong, M.C.S.; Goggins, W.B; Yip, B.H.K.; Fung, F.D.H.; Leung, C.; Fang, Y.; Wong, S.Y.S.; Ng, C.F. Incidence and mortality of kidney cancer: Temporal patterns and global trends in 39 countries. Sci Rep., 2017, 7(1), 15698.
[http://dx.doi.org/10.1038/s41598-017-15922-4]
[5]
Abreu, D.; Carvalhal, G.; Gueglio, G.; Tobia, I.; Garcia, P.; Zuñiga, A.; Meza, L.; Bengió, R.; Scorticati, C.; Castillejos, R.; Rodriguez, F.; Autran, A.M.; Gonzales, C.; Gadu, J.; Nolazco, A.; Ameri, C.; Zampolli, H.; Langenhin, R.; Muguruza, D.; Machado, M.T.; Mingote, P.; Yandian, J.; Clavijo, J.; Nogueira, L.; Clark, O.; Secin, F.; Rovegno, A.; Vilas, A.; Barrios, E.; Decia, R.; Guimarães, G.; Glina, S.; Pal, S.K.; Rodriguez, O.; Palou, J.; Spiess, P.; Lara, P.N., Jr; Linehan, W.M.; Pastore, A.L.; Zequi, S.C. Prognostic factors in de novo metastatic renal cell carcinoma: A report from the latin American renal cancer group. JCO Glob. Oncol., 2021, 7(7), 671-685.
[http://dx.doi.org/10.1200/GO.20.00621] [PMID: 33974442]
[6]
Goyal, R.; Gersbach, E.; Yang, X.J.; Rohan, S.M. Differential diagnosis of renal tumors with clear cytoplasm: Clinical relevance of renal tumor subclassification in the era of targeted therapies and personalized medicine. Arch. Pathol. Lab. Med., 2013, 137(4), 467-480.
[http://dx.doi.org/10.5858/arpa.2012-0085-RA] [PMID: 23544936]
[7]
Pal, S.K.; Ghate, S.R.; Li, N.; Swallow, E.; Peeples, M.; Zichlin, M.L.; Perez, J.R.; Agarwal, N.; Vogelzang, N.J. Real-world survival outcomes and prognostic factors among patients receiving first targeted therapy for advanced renal cell carcinoma: A SEER-Medicare database analysis. Clin. Genitourin. Cancer, 2017, 15(4), e573-e582.
[http://dx.doi.org/10.1016/j.clgc.2016.12.005] [PMID: 28139444]
[8]
Cooley, L.S.; Rudewicz, J.; Souleyreau, W.; Emanuelli, A.; Alvarez-Arenas, A.; Clarke, K.; Falciani, F.; Dufies, M.; Lambrechts, D.; Modave, E.; Chalopin-Fillot, D.; Pineau, R.; Ambrosetti, D.; Bernhard, J.C.; Ravaud, A.; Négrier, S.; Ferrero, J.M.; Pagès, G.; Benzekry, S.; Nikolski, M.; Bikfalvi, A. Experimental and computational modeling for signature and biomarker discovery of renal cell carcinoma progression. Mol. Cancer., 2021, 20(1), 136.
[http://dx.doi.org/10.1186/s12943-021-01416-5]
[9]
Hua, H.; Kong, Q.; Zhang, H.; Wang, J.; Luo, T.; Jiang, Y. Targeting mTOR for cancer therapy. J. Hematol. Oncol., 2019, 12(1), 71.
[http://dx.doi.org/10.1186/s13045-019-0754-1]
[10]
Aweys, H.; Lewis, D.; Sheriff, M.; Rabbani, R.D.; Lapitan, P.; Sanchez, E.; Papadopoulos, V.; Ghose, A.; Boussios, S. Renal cell cancer-insights in drug resistance mechanisms. Anticancer Res., 2023, 43(11), 4781-4792.
[http://dx.doi.org/10.21873/anticanres.16675] [PMID: 37909991]
[11]
Rini, B.I.; Atkins, M.B. Resistance to targeted therapy in renal-cell carcinoma. Lancet Oncol., 2009, 10(10), 992-1000.
[http://dx.doi.org/10.1016/S1470-2045(09)70240-2] [PMID: 19796751]
[12]
Makhov, P.; Joshi, S.; Ghatalia, P.; Kutikov, A.; Uzzo, R.G.; Kolenko, V.M. Resistance to systemic therapies in clear cell renal cell carcinoma: Mechanisms and management strategies. Mol. Cancer Ther., 2018, 17(7), 1355-1364.
[http://dx.doi.org/10.1158/1535-7163.MCT-17-1299] [PMID: 29967214]
[13]
Sharma, R.; Kadife, E.; Myers, M.; Kannourakis, G.; Prithviraj, P.; Ahmed, N. Determinants of resistance to VEGF-TKI and immune checkpoint inhibitors in metastatic renal cell carcinoma. J. Exp. Clin. Cancer. Res., 2021, 40(1), 186.
[http://dx.doi.org/10.1186/s13046-021-01961-3]
[14]
Folberg, R.; Maniotis, A.J. Vasculogenic mimicry. Acta Pathol. Microbiol. Scand. Suppl., 2004, 112(7-8), 508-525.
[http://dx.doi.org/10.1111/j.1600-0463.2004.apm11207-0810.x] [PMID: 15563313]
[15]
Soda, Y.; Marumoto, T.; Friedmann-Morvinski, D.; Soda, M.; Liu, F.; Michiue, H.; Pastorino, S.; Yang, M.; Hoffman, R.M.; Kesari, S.; Verma, I.M. Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc. Natl. Acad. Sci. USA, 2011, 108(11), 4274-4280.
[http://dx.doi.org/10.1073/pnas.1016030108] [PMID: 21262804]
[16]
Pezzella, F.; Ribatti, D. Vascular co-option and vasculogenic mimicry mediate resistance to antiangiogenic strategies. Cancer Rep., 2022, 5(12), e1318.
[http://dx.doi.org/10.1002/cnr2.1318] [PMID: 33295149]
[17]
Tsai, P.H.; Cheng, C.H.; Lin, C.Y.; Huang, Y.T.; Lee, L.T.; Kandaswami, C.C.; Lin, Y.C.; Lee, K.P.H.; Hung, C.C.; Hwang, J.J.; Ke, F.C.; Chang, G.D.; Lee, M.T. Dietary flavonoids luteolin and quercetin suppressed cancer stem cell properties and metastatic potential of isolated prostate cancer cells. Anticancer Res., 2016, 36(12), 6367-6380.
[http://dx.doi.org/10.21873/anticanres.11234] [PMID: 27919958]
[18]
Zhang, Y.; Xu, J.; Xu, Z.; Wang, Y.; Wu, S.; Wu, L.; Song, H.; Zhou, L. Expression of vimentin and Oct-4 in gallbladder adenocarcinoma and their relationship with vasculogenic mimicry and their clinical significance. Int. J. Clin. Exp. Pathol., 2018, 11(7), 3618-3627.
[19]
Lin, H.; Pan, J.; Zhang, F.; Huang, B.; Chen, X.; Zhuang, J.; Wang, H.; Mo, C.; Wang, D.; Qiu, S. Matrix metalloproteinase-9 is required for vasculogenic mimicry by clear cell renal carcinoma cells. Urol. Oncol., 2015, 33(4), 168.e9-168.e16.
[http://dx.doi.org/10.1016/j.urolonc.2014.12.007] [PMID: 25618297]
[20]
Lin, H.; Hong, Y.; Huang, B.; Liu, X.; Zheng, J.; Qiu, S. Vimentin overexpressions induced by cell hypoxia promote vasculogenic mimicry by renal cell carcinoma cells. BioMed Res. Int., 2019, 2019, 1-12.
[http://dx.doi.org/10.1155/2019/7259691] [PMID: 31428643]
[21]
Bai, J.; Yeh, S.; Qiu, X.; Hu, L.; Zeng, J.; Cai, Y.; Zuo, L.; Li, G.; Yang, G.; Chang, C. TR4 nuclear receptor promotes clear cell renal cell carcinoma (ccRCC) vasculogenic mimicry (VM) formation and metastasis via altering the miR490-3p/vimentin signals. Oncogene, 2018, 37(44), 5901-5912.
[http://dx.doi.org/10.1038/s41388-018-0269-1] [PMID: 29973687]
[22]
You, B.; Sun, Y.; Luo, J.; Wang, K.; Liu, Q.; Fang, R.; Liu, B.; Chou, F.; Wang, R.; Meng, J.; Huang, C.P.; Yeh, S.; Chang, C.; Xu, W. Androgen receptor promotes renal cell carcinoma (RCC) vasculogenic mimicry (VM) via altering TWIST1 nonsense-mediated decay through lncRNA-TANAR. Oncogene, 2021, 40(9), 1674-1689.
[http://dx.doi.org/10.1038/s41388-020-01616-1] [PMID: 33510354]
[23]
Goel, A.; Kunnumakkara, A.B.; Aggarwal, B.B. Curcumin as “Curecumin”: From kitchen to clinic. Biochem. Pharmacol., 2008, 75(4), 787-809.
[http://dx.doi.org/10.1016/j.bcp.2007.08.016] [PMID: 17900536]
[24]
Maheshwari, R.K.; Singh, A.K.; Gaddipati, J.; Srimal, R.C. Multiple biological activities of curcumin: A short review. Life Sci., 2006, 78(18), 2081-2087.
[http://dx.doi.org/10.1016/j.lfs.2005.12.007] [PMID: 16413584]
[25]
Esatbeyoglu, T.; Huebbe, P.; Ernst, I.M.A.; Chin, D.; Wagner, A.E.; Rimbach, G. Curcumin--from molecule to biological function. Angew. Chem. Int. Ed., 2012, 51(22), 5308-5332.
[http://dx.doi.org/10.1002/anie.201107724] [PMID: 22566109]
[26]
Li, Y.; Zhang, T. Targeting cancer stem cells by curcumin and clinical applications. Cancer Lett., 2014, 346(2), 197-205.
[http://dx.doi.org/10.1016/j.canlet.2014.01.012] [PMID: 24463298]
[27]
Guo, Y.; Wang, T.; Fu, F.F.; El-Kassaby, Y.A.; Wang, G. Temporospatial flavonoids metabolism variation in Ginkgo biloba leaves. Front. Genet., 2020, 11, 589326.
[http://dx.doi.org/10.3389/fgene.2020.589326] [PMID: 33329734]
[28]
Anand, P.; Sundaram, C.; Jhurani, S.; Kunnumakkara, A.B.; Aggarwal, B.B. Curcumin and cancer: An “old-age” disease with an “age-old” solution. Cancer Lett., 2008, 267(1), 133-164.
[http://dx.doi.org/10.1016/j.canlet.2008.03.025] [PMID: 18462866]
[29]
Kunnumakkara, A.B.; Bordoloi, D.; Padmavathi, G.; Monisha, J.; Roy, N.K.; Prasad, S.; Aggarwal, B.B. Curcumin, the golden nutraceutical: Multitargeting for multiple chronic diseases. Br. J. Pharmacol., 2017, 174(11), 1325-1348.
[http://dx.doi.org/10.1111/bph.13621] [PMID: 27638428]
[30]
Kuttikrishnan, S.; Siveen, K.S.; Prabhu, K.S.; Khan, A.Q.; Ahmed, E.I.; Akhtar, S.; Ali, T.A.; Merhi, M.; Dermime, S.; Steinhoff, M.; Uddin, S. Curcumin induces apoptotic cell death via inhibition of PI3-Kinase/AKT pathway in B-precursor acute lymphoblastic leukemia. Front Oncol., 2019, 19(9), 484.
[31]
Mortezaee, K.; Salehi, E.; Mirtavoos-mahyari, H.; Motevaseli, E.; Najafi, M.; Farhood, B.; Rosengren, R.J.; Sahebkar, A. Mechanisms of apoptosis modulation by curcumin: Implications for cancer therapy. J. Cell. Physiol., 2019, 234(8), 12537-12550.
[http://dx.doi.org/10.1002/jcp.28122] [PMID: 30623450]
[32]
Shao, Z.M.; Shen, Z.Z.; Liu, C.H.; Sartippour, M.R.; Go, V.L.; Heber, D.; Nguyen, M. Curcumin exerts multiple suppressive effects on human breast carcinoma cells. Int. J. Cancer, 2002, 98(2), 234-240.
[http://dx.doi.org/10.1002/ijc.10183] [PMID: 11857414]
[33]
Killian, P.H.; Kronski, E.; Michalik, K.M.; Barbieri, O.; Astigiano, S.; Sommerhoff, C.P.; Pfeffer, U.; Nerlich, A.G.; Bachmeier, B.E. Curcumin inhibits prostate cancer metastasis in vivo by targeting the inflammatory cytokines CXCL1 and -2. Carcinogenesis, 2012, 33(12), 2507-2519.
[http://dx.doi.org/10.1093/carcin/bgs312] [PMID: 23042094]
[34]
Bhandarkar, S.S.; Arbiser, J.L. Curcumin as an inhibitor of angiogenesis. Adv. Exp. Med. Biol., 2007, 595, 185-195.
[http://dx.doi.org/10.1007/978-0-387-46401-5_7] [PMID: 17569211]
[35]
Wang, T.Y.; Chen, J.X. Effects of curcumin on vessel formation insight into the pro- and antiangiogenesis of curcumin. Evid. Based Complement. Alternat. Med., 2019, 19, 1390795.
[36]
Chen, L.X.; He, Y.J.; Zhao, S.Z.; Wu, J.G.; Wang, J.T.; Zhu, L.M.; Lin, T.T.; Sun, B.C.; Li, X.R. Inhibition of tumor growth and vasculogenic mimicry by curcumin through down-regulation of the EphA2/PI3K/MMP pathway in a murine choroidal melanoma model. Cancer Biol. Ther., 2011, 11(2), 229-235.
[http://dx.doi.org/10.4161/cbt.11.2.13842] [PMID: 21084858]
[37]
Liang, Y.; Huang, M.; Li, J.; Sun, X.; Jiang, X.; Li, L.; Ke, Y. Curcumin inhibits vasculogenic mimicry through the downregulation of erythropoietin-producing hepatocellular carcinoma-A2, phosphoinositide 3-kinase and matrix metalloproteinase-2. Oncol. Lett., 2014, 8(4), 1849-1855.
[http://dx.doi.org/10.3892/ol.2014.2401] [PMID: 25202424]
[38]
Chiablaem, K.; Lirdprapamongkol, K.; Keeratichamroen, S.; Surarit, R.; Svasti, J. Curcumin suppresses vasculogenic mimicry capacity of hepatocellular carcinoma cells through STAT3 and PI3K/AKT inhibition. Anticancer Res., 2014, 34(4), 1857-1864.
[PMID: 24692720]
[39]
Hu, A.; Huang, J.J.; Jin, X.J.; Li, J.P.; Tang, Y.J.; Huang, X.F.; Cui, H.J.; Xu, W.H.; Sun, G.B. Curcumin suppresses invasiveness and vasculogenic mimicry of squamous cell carcinoma of the larynx through the inhibition of JAK-2/STAT-3 signaling pathway. Am. J. Cancer Res., 2014, 5(1), 278-88.
[40]
Song, Z.; Chen, L.; Pang, S.; Yan, B. Molecular genetic study on GATA5 gene promoter in acute myocardial infarction. PLoS One, 2021, 16(3), e0248203.
[http://dx.doi.org/10.1371/journal.pone.0248203]
[41]
Pavía-Jiménez, A.; Tcheuyap, V.T.; Brugarolas, J. Establishing a human renal cell carcinoma tumorgraft platform for preclinical drug testing. Nat. Protoc., 2014, 9(8), 1848-1859.
[http://dx.doi.org/10.1038/nprot.2014.108] [PMID: 25010905]
[42]
Gao, Y.; Shi, Q.; Xu, S.; Du, C.; Liang, L.; Wu, K.; Wang, K.; Wang, X.; Chang, L.; He, D.; Guo, P. Curcumin promotes KLF5 proteasome degradation through downregulating YAP/TAZ in bladder cancer cells. Int. J. Mol. Sci., 2014, 15(9), 15173-15187.
[http://dx.doi.org/10.3390/ijms150915173] [PMID: 25170806]
[43]
Kim, H.S.; Won, Y.J.; Shim, J.H.; Kim, H.J.; Kim, J.; Hong, H.N.; Kim, B.S. Morphological characteristics of vasculogenic mimicry and its correlation with EphA2 expression in gastric adenocarcinoma. Sci. Rep., 2019, 9(1), 3414.
[http://dx.doi.org/10.1038/s41598-019-40265-7]
[44]
Yang, J.P.; Liao, Y.D.; Mai, D.M.; Xie, P.; Qiang, Y.Y.; Zheng, L.S.; Wang, M.Y.; Mei, Y.; Meng, D.F.; Xu, L.; Cao, L.; Yang, Q.; Yang, X.X.; Wang, W.B.; Peng, L.X.; Huang, B.J.; Qian, C.N. Tumor vasculogenic mimicry predicts poor prognosis in cancer patients: A meta-analysis. Angiogenesis, 2016, 19(2), 191-200.
[http://dx.doi.org/10.1007/s10456-016-9500-2] [PMID: 26899730]
[45]
Vallianou, N.G.; Evangelopoulos, A.; Schizas, N.; Kazazis, C. Potential anticancer properties and mechanisms of action of curcumin. Anticancer Res., 2015, 35(2), 645-651.
[PMID: 25667441]
[46]
Hassan, F.U.; Rehman, M.S.; Khan, M.S.; Ali, M.A.; Javed, A.; Nawaz, A.; Yang, C. Curcumin as an alternative epigenetic modulator: Mechanism of action and potential effects. Front. Genet., 2019, 10, 514.
[http://dx.doi.org/10.3389/fgene.2019.00514]
[47]
Delgado-Bellido, D.; Serrano-Saenz, S.; Fernández-Cortés, M.; Oliver, F.J. Vasculogenic mimicry signaling revisited: Focus on non-vascular VE-cadherin. Mol. Cancer, 2017, 16(1), 65.
[http://dx.doi.org/10.1186/s12943-017-0631-x] [PMID: 28320399]
[48]
Delgado-Bellido, D.; Zamudio-Martínez, E.; Fernández-Cortés, M.; Herrera-Campos, A.B.; Olmedo-Pelayo, J.; Perez, C.J.; Expósito, J.; de Álava, E.; Amaral, A.T.; Valle, F.O.; Diaz, A.G.; Oliver, F.J. VE-Cadherin modulates β-catenin/TCF-4 to enhance vasculogenic mimicry. Cell Death Dis., 2023, 14(14)(2), 135.
[49]
Gong, J.; Maia, M.C.; Dizman, N.; Govindarajan, A.; Pal, S.K. Metastasis in renal cell carcinoma: Biology and implications for therapy. Asian J. Urol., 2016, 3(4), 286-292.
[http://dx.doi.org/10.1016/j.ajur.2016.08.006] [PMID: 29264197]
[50]
Folkman, J. Role of angiogenesis in tumor growth and metastasis. Semin. Oncol., 2002, 29(S6), 15-18.
[http://dx.doi.org/10.1016/S0093-7754(02)70065-1] [PMID: 12516034]
[51]
Tamaskar, I.; Dhillon, J.; Pili, R. Resistance to angiogenesis inhibitors in renal cell carcinoma. Clin. Adv. Hematol. Oncol., 2011, 9(2), 101-110.
[PMID: 22173604]
[52]
McGuire, T.F.; Sajithlal, G.B.; Lu, J.; Nicholls, R.D.; Prochownik, E.V. In vivo evolution of tumor-derived endothelial cells. PLoS One, 2012, 7(5), e37138.
[http://dx.doi.org/10.1371/journal.pone.0037138] [PMID: 22623986]
[53]
Liu, Z.; Ying, Y. The inhibitory effect of curcumin on virus-induced cytokine storm and its potential use in the associated severe pneumonia. Front. Cell. Dev. Biol., 2020, 8, 479.
[http://dx.doi.org/10.3389/fcell.2020.00479]
[54]
Pany, S.; You, Y.; Das, J. Curcumin inhibits protein kinase cα activity by binding to its c1 domain. Biochem., 2016, 55(45), 6327-6336.
[http://dx.doi.org/10.1021/acs.biochem.6b00932]
[55]
Giordano, A.; Tommonaro, G. Curcumin and cancer. Nutrients, 2019, 11(10), 2376.
[http://dx.doi.org/10.3390/nu11102376] [PMID: 31590362]
[56]
Yamada, M.; Yanaba, K.; Hasegawa, M.; Matsushita, Y.; Horikawa, M.; Komura, K.; Matsushita, T.; Kawasuji, A.; Fujita, T.; Takehara, K.; Steeber, D.A.; Tedder, T.F.; Sato, S. Regulation of local and metastatic host-mediated anti-tumour mechanisms by L -selectin and intercellular adhesion molecule-1. Clin. Exp. Immunol., 2005, 143(2), 216-227.
[http://dx.doi.org/10.1111/j.1365-2249.2005.02989.x] [PMID: 16412045]
[57]
Paschos, K.A.; Canovas, D.; Bird, N.C. The role of cell adhesion molecules in the progression of colorectal cancer and the development of liver metastasis. Cell. Signal., 2009, 21(5), 665-674.
[http://dx.doi.org/10.1016/j.cellsig.2009.01.006] [PMID: 19167485]
[58]
Usami, Y.; Ishida, K.; Sato, S.; Kishino, M.; Kiryu, M.; Ogawa, Y.; Okura, M.; Fukuda, Y.; Toyosawa, S. Intercellular adhesion molecule-1 (ICAM-1) expression correlates with oral cancer progression and induces macrophage/cancer cell adhesion. Int. J. Cancer, 2013, 133(3), 568-578.
[http://dx.doi.org/10.1002/ijc.28066] [PMID: 23364881]
[59]
He, X.; Lei, S.; Zhang, Q.; Ma, L.; Li, N.; Wang, J. Deregulation of cell adhesion molecules is associated with progression and poor outcomes in endometrial cancer: Analysis of The Cancer Genome Atlas data. Oncol. Lett., 2020, 19(3), 1906-1914.
[http://dx.doi.org/10.3892/ol.2020.11295] [PMID: 32194686]
[60]
A Fry, E.; Inoue, K. Aberrant expression of ETS1 and ETS2 proteins in cancer. Cancer Rep. Rev., 2018, 2(3)
[http://dx.doi.org/10.15761/CRR.1000151] [PMID: 29974077]
[61]
Tsutsumi, S.; Kuwano, H.; Asao, T.; Nagashima, K.; Shimura, T.; Mochiki, E. Expression of Ets-1 angiogenesis-related protein in gastric cancer. Cancer Lett., 2000, 160(1), 45-50.
[http://dx.doi.org/10.1016/S0304-3835(00)00559-0] [PMID: 11098083]
[62]
Furlan, A.; Vercamer, C.; Heliot, L.; Wernert, N.; Desbiens, X.; Pourtier, A. Ets-1 drives breast cancer cell angiogenic potential and interactions between breast cancer and endothelial cells. Int. J. Oncol., 2019, 54(1), 29-40.
[PMID: 30365153]
[63]
Zhou, X.; Zhou, R.; Zhou, H.; Li, Q.; Hong, J.; Meng, R.; Zhu, F.; Zhang, S.; Dai, X.; Peng, G.; Wu, G.; Li, Z. ETS-1 induces endothelial-like differentiation and promotes metastasis in non-small cell lung cancer. Cell. Physiol. Biochem., 2018, 45(5), 1827-1839.
[http://dx.doi.org/10.1159/000487874] [PMID: 29510376]
[64]
Delgado-Bellido, D.; Fernández-Cortés, M.; Rodríguez, M.I.; Serrano-Sáenz, S.; Carracedo, A.; Garcia-Diaz, A.; Oliver, F.J. VE-cadherin promotes vasculogenic mimicry by modulating kaiso-dependent gene expression. Cell Death Differ., 2019, 26(2), 348-361.
[http://dx.doi.org/10.1038/s41418-018-0125-4] [PMID: 29786069]
[65]
Cathcart, J.; Pulkoski-Gross, A.; Cao, J. Targeting matrix metalloproteinases in cancer: Bringing new life to old ideas. Genes Dis., 2015, 2(1), 26-34.
[http://dx.doi.org/10.1016/j.gendis.2014.12.002] [PMID: 26097889]
[66]
Le Bras, A.; Lionneton, F.; Mattot, V.; Lelièvre, E.; Caetano, B.; Spruyt, N.; Soncin, F. HIF-2α specifically activates the VE-cadherin promoter independently of hypoxia and in synergy with Ets-1 through two essential ETS-binding sites. Oncogene, 2007, 26(53), 7480-7489.
[http://dx.doi.org/10.1038/sj.onc.1210566] [PMID: 17563748]
[67]
Befani, C.; Liakos, P. The role of hypoxia-inducible factor-2 alpha in angiogenesis. J. Cell. Physiol., 2018, 233(12), 9087-9098.
[http://dx.doi.org/10.1002/jcp.26805] [PMID: 29968905]
[68]
Shishodia, S.; Singh, T.; Chaturvedi, M.M. Modulation of transcription factors by curcumin. Adv. Exp. Med. Biol., 2007, 595, 127-148.
[http://dx.doi.org/10.1007/978-0-387-46401-5_4] [PMID: 17569208]
[69]
Ghosh, S.; Basu, M.; Roy, S.S. ETS-1 protein regulates vascular endothelial growth factor-induced matrix metalloproteinase-9 and matrix metalloproteinase-13 expression in human ovarian carcinoma cell line SKOV-3. J. Biol. Chem., 2012, 287(18), 15001-15015.
[http://dx.doi.org/10.1074/jbc.M111.284034] [PMID: 22270366]
[70]
Nazir, S.U.; Kumar, R.; Singh, A.; Khan, A.; Tanwar, P.; Tripathi, R.; Mehrotra, R.; Hussain, S. Breast cancer invasion and progression by MMP-9 through Ets-1 transcription factor. Gene., 2019, 711, 143952.
[http://dx.doi.org/10.1016/j.gene.2019.143952]
[71]
Fernández-Cortés, M.; Delgado-Bellido, D.; Oliver, F.J. Vasculogenic mimicry: Become an endothelial cell "but not so much". Front Oncol., 2019, 22(9), 803.
[72]
Huizhi, S.; Nan, Y.; Siqi, C.; Linqi, L.; Shiqi, L.; Zhao, Y.; Guanjie, S.; Danfang, Z.; Zhi, Y. Cancer stem-like cells directly participate in vasculogenic mimicry channels in triple-negative breast cancer. Cancer Biol. Med., 2019, 16(2), 299-311.
[http://dx.doi.org/10.20892/j.issn.2095-3941.2018.0209] [PMID: 31516750]
[73]
Lizárraga-Verdugo, E.; Avendaño-Félix, M.; Bermúdez, M.; Ramos-Payán, R.; Pérez-Plasencia, C.; Aguilar-Medina, M. Cancer stem cells and its role in angiogenesis and vasculogenic mimicry in gastrointestinal cancers. Front. Oncol., 2020, 10, 413.
[http://dx.doi.org/10.3389/fonc.2020.00413]
[74]
Cheng, T.; Zhang, S.; Xia, T.; Zhang, Y.; Ji, Y.; Pan, S.; Xie, H.; Ren, Q.; You, Y.; You, B. EBV promotes vascular mimicry of dormant cancer cells by potentiating stemness and EMT. Exp Cell. Res., 2022, 421(2), 113403.
[http://dx.doi.org/10.1016/j.yexcr.2022.113403]

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