Generic placeholder image

Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Research Article

Integrated Analysis of the Expression, Involved Functions, and Regulatory Network of RUNX3 in Melanoma

Author(s): Zhang Feng, Yanxin Liu and Huaxia Chen*

Volume 25, Issue 9, 2022

Published on: 18 January, 2022

Page: [1552 - 1564] Pages: 13

DOI: 10.2174/1386207324666210816121833

Price: $65

Abstract

Background: As a tumor suppressor or oncogenic gene, abnormal expression of RUNX family transcription factor 3 (RUNX3) has been reported in various cancers.

Introduction: This study aimed to investigate the role of RUNX3 in melanoma.

Methods: The expression level of RUNX3 in melanoma tissues was analyzed by immunohistochemistry and the Oncomine database. Based on microarray datasets GSE3189 and GSE7553, differentially expressed genes (DEGs) in melanoma samples were screened, followed by functional enrichment analysis. Gene Set Enrichment Analysis (GSEA) was performed for RUNX3. DEGs that co-expressed with RUNX3 were analyzed, and the transcription factors (TFs) of RUNX3 and its co-expressed genes were predicted. The protein-protein interactions (PPIs) for RUNX3 were analyzed utilizing the GeneMANIA database. MicroRNAs (miRNAs) that could target RUNX3 expression, were predicted.

Results: RUNX3 expression was significantly up-regulated in melanoma tissues. GSEA showed that RUNX3 expression was positively correlated with melanogenesis and melanoma pathways. Eleven DEGs showed significant co-expression with RUNX3 in melanoma, for example, TLE4 was negatively co-expressed with RUNX3. RUNX3 was identified as a TF that regulated the expression of both itself and its co-expressed genes. PPI analysis showed that 20 protein-encoding genes interacted with RUNX3, among which 9 genes were differentially expressed in melanoma, such as CBFB and SMAD3. These genes were significantly enriched in transcriptional regulation by RUNX3, RUNX3 regulates BCL2L11 (BIM) transcription, regulation of I-kappaB kinase/NFkappaB signaling, and signaling by NOTCH. A total of 31 miRNAs could target RUNX3, such as miR-326, miR-330-5p, and miR-373-3p.

Conclusion: RUNX3 expression was up-regulated in melanoma and was implicated in the development of melanoma.

Keywords: Melanoma, RUNX family transcription factor 3, microRNAs, melanogenesis, GSEA, PPI analysis.

Graphical Abstract

[1]
Swetter, S.M.; Tsao, H.; Bichakjian, C.K.; Curiel-Lewandrowski, C.; Elder, D.E.; Gershenwald, J.E.; Guild, V.; Grant-Kels, J.M.; Halpern, A.C.; Johnson, T.M.; Sober, A.J.; Thompson, J.A.; Wisco, O.J.; Wyatt, S.; Hu, S.; Lamina, T. Guidelines of care for the management of primary cutaneous melanoma. J. Am. Acad. Dermatol., 2019, 80(1), 208-250.
[http://dx.doi.org/10.1016/j.jaad.2018.08.055] [PMID: 30392755]
[2]
Schadendorf, D.; van Akkooi, A.C.J.; Berking, C.; Griewank, K.G.; Gutzmer, R.; Hauschild, A.; Stang, A.; Roesch, A.; Ugurel, S. Melanoma. Lancet, 2018, 392(10151), 971-984.
[http://dx.doi.org/10.1016/S0140-6736(18)31559-9] [PMID: 30238891]
[3]
Leonardi, G.C.; Falzone, L.; Salemi, R.; Zanghì, A.; Spandidos, D.A.; Mccubrey, J.A.; Candido, S.; Libra, M. Cutaneous melanoma: From pathogenesis to therapy (Review). Int. J. Oncol., 2018, 52(4), 1071-1080.
[http://dx.doi.org/10.3892/ijo.2018.4287] [PMID: 29532857]
[4]
Lugović-Mihić, L.; Ćesić, D.; Vuković, P.; Novak Bilić, G.; Šitum, M.; Špoljar, S. Melanoma development: current knowledge on melanoma pathogenesis. Acta Dermatovenerol. Croat., 2019, 27(3), 163-168.
[PMID: 31542060]
[5]
Hartman, R.I.; Lin, J.Y. Cutaneous Melanoma-A review in detection, staging, and management. Hematol. Oncol. Clin. North Am., 2019, 33(1), 25-38.
[http://dx.doi.org/10.1016/j.hoc.2018.09.005] [PMID: 30497675]
[6]
Moran, B.; Silva, R.; Perry, A.S.; Gallagher, W.M. Epigenetics of malignant melanoma. Semin. Cancer Biol., 2018, 51, 80-88.
[7]
Wouters, J.; Kalender-Atak, Z.; Minnoye, L.; Spanier, K.I.; De Waegeneer, M.; Bravo González-Blas, C.; Mauduit, D.; Davie, K.; Hulselmans, G.; Najem, A.; Dewaele, M.; Pedri, D.; Rambow, F.; Makhzami, S.; Christiaens, V.; Ceyssens, F.; Ghanem, G.; Marine, J.C.; Poovathingal, S.; Aerts, S. Robust gene expression programs underlie recurrent cell states and phenotype switching in melanoma. Nat. Cell Biol., 2020, 22(8), 986-998.
[http://dx.doi.org/10.1038/s41556-020-0547-3] [PMID: 32753671]
[8]
Ayachi, O.; Barlin, M.; Broxtermann, P.N.; Kashkar, H.; Mauch, C.; Zigrino, P. The X-linked inhibitor of apoptosis protein (XIAP) is involved in melanoma invasion by regulating cell migration and survival. Cell Oncol. (Dordr.), 2019, 42(3), 319-329.
[http://dx.doi.org/10.1007/s13402-019-00427-1] [PMID: 30778852]
[9]
Boto, P.; Csuth, T.I.; Szatmari, I. RUNX3-Mediated immune cell development and maturation. Crit. Rev. Immunol., 2018, 38(1), 63-78.
[http://dx.doi.org/10.1615/CritRevImmunol.2018025488] [PMID: 29717663]
[10]
Levanon, D.; Bettoun, D.; Harris-Cerruti, C.; Woolf, E.; Negreanu, V.; Eilam, R.; Bernstein, Y.; Goldenberg, D.; Xiao, C.; Fliegauf, M.; Kremer, E.; Otto, F.; Brenner, O.; Lev-Tov, A.; Groner, Y. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J., 2002, 21(13), 3454-3463.
[http://dx.doi.org/10.1093/emboj/cdf370] [PMID: 12093746]
[11]
Whittle, M.C.; Izeradjene, K.; Rani, P.G.; Feng, L.; Carlson, M.A.; DelGiorno, K.E.; Wood, L.D.; Goggins, M.; Hruban, R.H.; Chang, A.E.; Calses, P.; Thorsen, S.M.; Hingorani, S.R. RUNX3 controls a metastatic switch in pancreatic ductal adenocarcinoma. Cell, 2015, 161(6), 1345-1360.
[http://dx.doi.org/10.1016/j.cell.2015.04.048] [PMID: 26004068]
[12]
Chen, F.; Bai, J.; Li, W.; Mei, P.; Liu, H.; Li, L.; Pan, Z.; Wu, Y.; Zheng, J. RUNX3 suppresses migration, invasion and angiogenesis of human renal cell carcinoma. PLoS One, 2013, 8(2)e56241
[http://dx.doi.org/10.1371/journal.pone.0056241] [PMID: 23457532]
[13]
Huang, B.; Qu, Z.; Ong, C.W.; Tsang, Y.H.; Xiao, G.; Shapiro, D.; Salto-Tellez, M.; Ito, K.; Ito, Y.; Chen, L.F. RUNX3 acts as a tumor suppressor in breast cancer by targeting estrogen receptor α. Oncogene, 2012, 31(4), 527-534.
[http://dx.doi.org/10.1038/onc.2011.252] [PMID: 21706051]
[14]
Chen, F.; Wang, M.; Bai, J.; Liu, Q.; Xi, Y.; Li, W.; Zheng, J. Role of RUNX3 in suppressing metastasis and angiogenesis of human prostate cancer. PLoS One, 2014, 9(1)e86917
[http://dx.doi.org/10.1371/journal.pone.0086917] [PMID: 24475196]
[15]
Jin, Z.; Han, Y.X.; Han, X.R. Loss of RUNX3 expression may contribute to poor prognosis in patients with chondrosarcoma. J. Mol. Histol., 2013, 44(6), 645-652.
[http://dx.doi.org/10.1007/s10735-013-9511-x] [PMID: 23666463]
[16]
Bledsoe, K.L.; McGee-Lawrence, M.E.; Camilleri, E.T.; Wang, X.; Riester, S.M.; van Wijnen, A.J.; Oliveira, A.M.; Westendorf, J.J. RUNX3 facilitates growth of Ewing sarcoma cells. J. Cell. Physiol., 2014, 229(12), 2049-2056.
[http://dx.doi.org/10.1002/jcp.24663] [PMID: 24812032]
[17]
Barghout, S.H.; Zepeda, N.; Vincent, K.; Azad, A.K.; Xu, Z.; Yang, C.; Steed, H.; Postovit, L.M.; Fu, Y. RUNX3 contributes to carboplatin resistance in epithelial ovarian cancer cells. Gynecol. Oncol., 2015, 138(3), 647-655.
[http://dx.doi.org/10.1016/j.ygyno.2015.07.009] [PMID: 26186909]
[18]
Kudo, Y.; Tsunematsu, T.; Takata, T. Oncogenic role of RUNX3 in head and neck cancer. J. Cell. Biochem., 2011, 112(2), 387-393.
[http://dx.doi.org/10.1002/jcb.22967] [PMID: 21268058]
[19]
Zhang, X.; Wang, L.; Zeng, X.; Fujita, T.; Liu, W. Runx3 inhibits melanoma cell migration through regulation of cell shape change. Cell Biol. Int., 2017, 41(9), 1048-1055.
[http://dx.doi.org/10.1002/cbin.10824] [PMID: 28699302]
[20]
Rhodes, D.R.; Yu, J.; Shanker, K.; Deshpande, N.; Varambally, R.; Ghosh, D.; Barrette, T.; Pandey, A.; Chinnaiyan, A.M. ONCOMINE: A cancer microarray database and integrated data-mining platform. Neoplasia, 2004, 6(1), 1-6.
[http://dx.doi.org/10.1016/S1476-5586(04)80047-2] [PMID: 15068665]
[21]
Yu, G.; Wang, L.G.; Han, Y.; He, Q.Y. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS, 2012, 16(5), 284-287.
[http://dx.doi.org/10.1089/omi.2011.0118] [PMID: 22455463]
[22]
Liberzon, A.; Birger, C.; Thorvaldsdóttir, H.; Ghandi, M.; Mesirov, J.P.; Tamayo, P. The molecular signatures database (MSigDB) hallmark gene set collection. Cell Syst., 2015, 1(6), 417-425.
[http://dx.doi.org/10.1016/j.cels.2015.12.004] [PMID: 26771021]
[23]
Franz, M.; Rodriguez, H.; Lopes, C.; Zuberi, K.; Montojo, J.; Bader, G.D.; Morris, Q. GeneMANIA update 2018. Nucleic Acids Res., 2018, 46(W1), W60-W64.
[http://dx.doi.org/10.1093/nar/gky311] [PMID: 29912392]
[24]
Zuberi, K.; Franz, M.; Rodriguez, H.; Montojo, J.; Lopes, C.T.; Bader, G.D.; Morris, Q. GeneMANIA prediction server 2013 update. Nucleic Acids Res., 2013, 41 Web Server issue), W115-22. [Web Server issue].
[PMID: 23794635]
[25]
Zhou, Y.; Zhou, B.; Pache, L.; Chang, M.; Khodabakhshi, A.H.; Tanaseichuk, O.; Benner, C.; Chanda, S.K. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat. Commun., 2019, 10(1), 1523.
[http://dx.doi.org/10.1038/s41467-019-09234-6] [PMID: 30944313]
[26]
Sticht, C.; De La Torre, C.; Parveen, A.; Gretz, N. miRWalk: An online resource for prediction of microRNA binding sites. PLoS One, 2018, 13(10)e0206239
[http://dx.doi.org/10.1371/journal.pone.0206239] [PMID: 30335862]
[27]
Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.; Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res., 2003, 13(11), 2498-2504.
[http://dx.doi.org/10.1101/gr.1239303] [PMID: 14597658]
[28]
Talantov, D.; Mazumder, A.; Yu, J.X.; Briggs, T.; Jiang, Y.; Backus, J.; Atkins, D.; Wang, Y. Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin. Cancer Res., 2005, 11(20), 7234-7242.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-0683] [PMID: 16243793]
[29]
Riker, AI; Enkemann, SA; Fodstad, O; Liu, S; Ren, S; Morris, C; Xi, Y; Howell, P; Metge, B; Samant, RS; Shevde, LA; Li, W; Eschrich, S; Daud, A; Ju, J; Matta, J The gene expression profiles of primary and metastatic melanoma yields a transition point of tumor progression and metastasis. BMC Med. Genomics., 2008, 1(13)
[http://dx.doi.org/10.1186/1755-8794-1-13] [PMID: 18442402]
[30]
Poser, I.; Bosserhoff, A.K. Transcription factors involved in development and progression of malignant melanoma. Histol. Histopathol., 2004, 19(1), 173-188.
[PMID: 14702186]
[31]
Thyagarajan, A.; Tsai, K.Y.; Sahu, R.P. MicroRNA heterogeneity in melanoma progression. Semin. Cancer Biol., 2019, 59, 208-220.
[32]
Lee, J.H.; Pyon, J.K.; Kim, D.W.; Lee, S.H.; Nam, H.S.; Kang, S.G.; Kim, C.H.; Lee, Y.J.; Chun, J.S.; Cho, M.K. Expression of RUNX3 in skin cancers. Clin. Exp. Dermatol., 2011, 36(7), 769-774.
[http://dx.doi.org/10.1111/j.1365-2230.2011.04069.x] [PMID: 21623876]
[33]
Kitago, M.; Martinez, S.R.; Nakamura, T.; Sim, M.S.; Hoon, D.S. Regulation of RUNX3 tumor suppressor gene expression in cutaneous melanoma. Clin. Cancer Res., 2009, 15(9), 2988-2994.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-3172] [PMID: 19336521]
[34]
Zhang, Z.; Chen, G.; Cheng, Y.; Martinka, M.; Li, G. Prognostic significance of RUNX3 expression in human melanoma. Cancer, 2011, 117(12), 2719-2727.
[http://dx.doi.org/10.1002/cncr.25838] [PMID: 21656750]
[35]
Kang, S.; Wang, Z.; Li, B.; Gao, X.; He, W.; Cao, S.; Cai, Y.; Chen, H. Anti-tumor effects of resveratrol on malignant melanoma is associated with promoter demethylation of RUNX3 gene. Pharmazie, 2019, 74(3), 163-167.
[PMID: 30961683]
[36]
Durst, K.L.; Hiebert, S.W. Role of RUNX family members in transcriptional repression and gene silencing. Oncogene, 2004, 23(24), 4220-4224.
[http://dx.doi.org/10.1038/sj.onc.1207122] [PMID: 15156176]
[37]
Jennings, B.H.; Ish-Horowicz, D. The Groucho/TLE/Grg family of transcriptional co-repressors. Genome Biol., 2008, 9(1), 205.
[http://dx.doi.org/10.1186/gb-2008-9-1-205] [PMID: 18254933]
[38]
Yarmus, M.; Woolf, E.; Bernstein, Y.; Fainaru, O.; Negreanu, V.; Levanon, D.; Groner, Y. Groucho/transducin-like enhancer-of-split (TLE)-dependent and -independent transcriptional regulation by Runx3. Proc. Natl. Acad. Sci. USA, 2006, 103(19), 7384-7389.
[http://dx.doi.org/10.1073/pnas.0602470103] [PMID: 16651517]
[39]
Qin, X.; Jiang, Q.; Matsuo, Y.; Kawane, T.; Komori, H.; Moriishi, T.; Taniuchi, I.; Ito, K.; Kawai, Y.; Rokutanda, S.; Izumi, S.; Komori, T. Cbfb regulates bone development by stabilizing Runx family proteins. J. Bone Miner. Res., 2015, 30(4), 706-714.
[http://dx.doi.org/10.1002/jbmr.2379] [PMID: 25262822]
[40]
Šuštić, T.; Bosdriesz, E.; van Wageningen, S.; Wessels, L.F.A.; Bernards, R. RUNX2/CBFB modulates the response to MEK inhibitors through activation of receptor tyrosine kinases in KRAS-mutant colorectal cancer. Transl. Oncol., 2020, 13(2), 201-211.
[http://dx.doi.org/10.1016/j.tranon.2019.10.006] [PMID: 31865182]
[41]
Malik, N.; Yan, H.; Moshkovich, N.; Palangat, M.; Yang, H.; Sanchez, V.; Cai, Z.; Peat, T.J.; Jiang, S.; Liu, C.; Lee, M.; Mock, B.A.; Yuspa, S.H.; Larson, D.; Wakefield, L.M.; Huang, J. The transcription factor CBFB suppresses breast cancer through orchestrating translation and transcription. Nat. Commun., 2019, 10(1), 019-10102.
[42]
Yokoyama, S.; Iwakami, Y.; Hang, Z.; Kin, R.; Zhou, Y.; Yasuta, Y.; Takahashi, A.; Hayakawa, Y.; Sakurai, H. Targeting PSMD14 inhibits melanoma growth through SMAD3 stabilization. Sci. Rep., 2020, 10(1), 19214-19214.
[http://dx.doi.org/10.1038/s41598-020-76373-y] [PMID: 33154524]
[43]
Bao, Y; Ding, Z; Zhao, P; Li, J; Chen, P; Zheng, J; Qian, Z Autophagy inhibition potentiates the anti-EMT effects of alteronol through TGF-β/Smad3 signaling in melanoma cells. Cell Death Dis., 2020, 11(4), 020-2419..
[44]
Xiao, Z.; Tian, Y.; Jia, Y.; Shen, Q.; Jiang, W.; Chen, G.; Shang, B.; Shi, M.; Wang, Z.; Zhao, X. RUNX3 inhibits the invasion and migration of esophageal squamous cell carcinoma by reversing the epithelial mesenchymal transition through TGF β/Smad signaling. Oncol. Rep., 2020, 43(4), 1289-1299.
[http://dx.doi.org/10.3892/or.2020.7508] [PMID: 32323849]
[45]
Sun, H.W.; Yang, G.L.; Wang, S.N.; Zhang, Y.J.; Ding, J.X.; Zhang, X.N. MicroRNA-92a regulates the development of cutaneous malignant melanoma by mediating FOXP1. Eur. Rev. Med. Pharmacol. Sci., 2019, 23(20), 8991-8999.
[PMID: 31696487]
[46]
Sehati, N.; Sadeghie, N.; Mansoori, B.; Mohammadi, A.; Shanehbandi, D.; Baradaran, B. MicroRNA-330 inhibits growth and migration of melanoma A375 cells: in vitro study. J. Cell. Biochem., 2020, 121(1), 458-467.
[http://dx.doi.org/10.1002/jcb.29211] [PMID: 31237010]
[47]
Yao, Y.; Zuo, J.; Wei, Y. Targeting of TRX2 by miR-330-3p in melanoma inhibits proliferation. Biomed. Pharmacother., 2018, 107, 1020-1029.
[http://dx.doi.org/10.1016/j.biopha.2018.08.058] [PMID: 30257313]
[48]
Long, J.; Menggen, Q.; Wuren, Q.; Shi, Q.; Pi, X. Long noncoding RNA taurine-upregulated gene1 (TUG1) promotes tumor growth and metastasis through TUG1/mir-129-5p/astrocyte-elevated gene-1 (AEG-1) axis in malignant melanoma. Med. Sci. Monit., 2018, 24, 157-1559.
[49]
Kang, K.; Zhang, J.; Zhang, X.; Chen, Z. MicroRNA-326 inhibits melanoma progression by targeting KRAS and suppressing the AKT and ERK signalling pathways. Oncol. Rep., 2018, 39(1), 401-410.
[PMID: 29115540]
[50]
Bai, X.; Yang, M.; Xu, Y. MicroRNA-373 promotes cell migration via targeting salt-inducible kinase 1 expression in melanoma. Exp. Ther. Med., 2018, 16(6), 4759-4764.
[http://dx.doi.org/10.3892/etm.2018.6784] [PMID: 30542430]
[51]
Zhu, Y.; Zhang, H.L.; Wang, Q.Y.; Chen, M.J.; Liu, L.B. Overexpression of microRNA-612 restrains the growth, invasion, and tumorigenesis of melanoma cells by targeting espin. Mol. Cells, 2018, 41(2), 119-126.
[PMID: 29385671]
[52]
Sun, L.; Wang, Q.; Gao, X.; Shi, D.; Mi, S.; Han, Q. MicroRNA-454 functions as an oncogene by regulating PTEN in uveal melanoma. FEBS Lett., 2015, 589(19 Pt B), 2791-2796.
[http://dx.doi.org/10.1016/j.febslet.2015.08.007] [PMID: 26296312]
[53]
Cui, L.; Li, Y.; Lv, X.; Li, J.; Wang, X.; Lei, Z.; Li, X. Expression of MicroRNA-301a and its functional roles in malignant melanoma. Cell. Physiol. Biochem., 2016, 40(1-2), 230-244.
[http://dx.doi.org/10.1159/000452540] [PMID: 27855389]
[54]
Ma, Y.; Duan, J.; Hao, X. Down-regulated HDAC3 elevates microRNA-495-3p to restrain epithelial-mesenchymal transition and oncogenicity of melanoma cells via reducing TRAF5. J. Cell. Mol. Med., 2020, 24(22), 12933-12944.
[http://dx.doi.org/10.1111/jcmm.15885] [PMID: 33048450]
[55]
Jin, C.; Wang, A.; Liu, L.; Wang, G.; Li, G.; Han, Z. miR-145-5p inhibits tumor occurrence and metastasis through the NF-κB signaling pathway by targeting TLR4 in malignant melanoma. J. Cell. Biochem., 2019, 30(10), 28388.
[http://dx.doi.org/10.1002/jcb.28388]
[56]
Li, J.R.; Wang, J.Q.; Gong, Q.; Fang, R.H.; Guo, Y.L. MicroRNA-328 inhibits proliferation of human melanoma cells by targeting TGFβ2. Asian Pac. J. Cancer Prev., 2015, 16(4), 1575-1579.
[http://dx.doi.org/10.7314/APJCP.2015.16.4.1575] [PMID: 25743834]
[57]
Xiang, S; Chen, H; Luo, X; An, B; Wu, W; Cao, S; Ruan, S; Wang, Z; Weng, L; Zhu, H; Liu, Q Isoliquiritigenin suppresses human melanoma growth by targeting miR-301b/LRIG1 signaling. J. Exp. Clin. Cancer Res, 2018, 37(1), 018-0844.
[58]
Zhang, J.; Liu, W.L.; Zhang, L.; Ge, R.; He, F.; Gao, T.Y.; Tian, Q.; Mu, X.; Chen, L.H.; Chen, W.; Li, X. MiR-637 suppresses melanoma progression through directly targeting P-REX2a and inhibiting PTEN/AKT signaling pathway. Cell. Mol. Biol., 2018, 64(11), 50-57.
[http://dx.doi.org/10.14715/cmb/2018.64.11.10] [PMID: 30213289]
[59]
Shen, S.; Yu, H.; Liu, X.; Liu, Y.; Zheng, J.; Wang, P.; Gong, W.; Chen, J.; Zhao, L.; Xue, Y. PIWIL1/piRNA-DQ593109 regulates the permeability of the blood-tumor barrier via the MEG3/miR-330-5p/RUNX3 axis. Mol. Ther. Nucleic Acids, 2018, 10, 412-425.
[60]
Li, X; Zhong, M; Wang, J; Wang, L; Lin, Z; Cao, Z; Huang, Z; Zhang, F; Li, Y; Liu, M; Ma, X. miR-301a promotes lung tumorigenesis by suppressing Runx3. Mol. Cancer, 2019, 18(1), 019-1024.
[61]
Paudel, D.; Zhou, W.; Ouyang, Y.; Dong, S.; Huang, Q.; Giri, R.; Wang, J.; Tong, X. MicroRNA-130b functions as a tumor suppressor by regulating RUNX3 in epithelial ovarian cancer. Gene, 2016, 586(1), 48-55.
[http://dx.doi.org/10.1016/j.gene.2016.04.001] [PMID: 27048832]
[62]
Wang, M.; Wang, X.; Liu, W. MicroRNA 130a 3p promotes the proliferation and inhibits the apoptosis of cervical cancer cells via negative regulation of RUNX3. Mol. Med. Rep., 2020, 22(4), 2990-3000.
[http://dx.doi.org/10.3892/mmr.2020.11368] [PMID: 32945424]
[63]
Lee, S.H.; Jung, Y.D.; Choi, Y.S.; Lee, Y.M. Targeting of RUNX3 by miR-130a and miR-495 cooperatively increases cell proliferation and tumor angiogenesis in gastric cancer cells. Oncotarget, 2015, 6(32), 33269-33278.
[http://dx.doi.org/10.18632/oncotarget.5037] [PMID: 26375442]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy