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http://dx.doi.org/10.4062/biomolther.2022.063

Snail Promotes Cancer Cell Proliferation via Its Interaction with the BIRC3  

Rho, Seung Bae (Division of Cancer Biology, Research Institute, National Cancer Center)
Byun, Hyun-Jung (BK21 FOUR Team and Integrated Research Institute for Drug Development, College of Pharmacy, Dongguk University)
Kim, Boh-Ram (BK21 FOUR Team and Integrated Research Institute for Drug Development, College of Pharmacy, Dongguk University)
Lee, Chang Hoon (BK21 FOUR Team and Integrated Research Institute for Drug Development, College of Pharmacy, Dongguk University)
Publication Information
Biomolecules & Therapeutics / v.30, no.4, 2022 , pp. 380-388 More about this Journal
Abstract
Snail is implicated in tumour growth and metastasis and is up-regulated in various human tumours. Although the role of Snails in epithelial-mesenchymal transition, which is particularly important in cancer metastasis, is well known, how they regulate tumour growth is poorly described. In this study, the possible molecular mechanisms of Snail in tumour growth were explored. Baculoviral inhibitor of apoptosis protein (IAP) repeat-containing protein 3 (BIRC3), a co-activator of cell proliferation during tumourigenesis, was identified as a Snail-binding protein via a yeast two-hybrid system. Since BIRC3 is important for cell survival, the effect of BIRC3 binding partner Snail on cell survival was investigated in ovarian cancer cell lines. Results revealed that Bax expression was activated, while the expression levels of anti-apoptotic proteins were markedly decreased by small interfering RNA (siRNA) specific for Snail (siSnail). siSnail, the binding partner of siBIRC3, activated the tumour suppressor function of p53 by promoting p53 protein stability. Conversely, BIRC3 could interact with Snail, for this reason, the possibility of BIRC3 involvement in EMT was investigated. BIRC3 overexpression resulted in a decreased expression of the epithelial marker and an increased expression of the mesenchymal markers. siSnail or siBIRC3 reduced the mRNA levels of matrix metalloproteinase (MMP)-2 and MMP-9. These results provide evidence that Snail promotes cell proliferation by interacting with BIRC3 and that BIRC3 might be involved in EMT via binding to Snail in ovarian cancer cells. Therefore, our results suggested the novel relevance of BIRC3, the binding partner of Snail, in ovarian cancer development.
Keywords
Snail; BIRC3; Yeast two-hybrid; P53; Proliferation; Ovarian cancer;
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1 Clarfield, L., Diamond, L. and Jacobson, M. (2022) Risk-reducing options for high-grade serous gynecologic malignancy in BRCA1/2. Curr. Oncol. 29, 2132-2140.   DOI
2 Dominguez, D., Montserrat-Sentis, B., Virgos-Soler, A., Guaita, S., Grueso, J., Porta, M., Puig, I., Baulida, J., Franci, C. and Garcia de Herreros, A. (2003) Phosphorylation regulates the subcellular location and activity of the snail transcriptional repressor. Mol. Cell. Biol. 23, 5078-5089.   DOI
3 Dong, S. M., Byun, H. J., Kim, B. R., Lee, S. H., Trink, B. and Rho, S. B. (2012) Tumor suppressor BLU enhances pro-apoptotic activity of sMEK1 through physical interaction. Cell. Signal. 24, 1208-1214.   DOI
4 Esposito, I., Kleeff, J., Abiatari, I., Shi, X., Giese, N., Bergmann, F., Roth, W., Friess, H. and Schirmacher, P. (2007) Overexpression of cellular inhibitor of apoptosis protein 2 is an early event in the progression of pancreatic cancer. J. Clin. Pathol. 60, 885-895.   DOI
5 Ferreira, C., Van Der Valk, P., Span, S., Jonker, J., Postmus, P., Kruyt, F. and Giaccone, G. (2001) Assessment of IAP (inhibitor of apoptosis) proteins as predictors of response to chemotherapy in advanced non-small-cell lung cancer patients. Ann. Oncol. 12, 799-805.   DOI
6 Bi, L., Zhang, C., Yao, Y. and He, Z. (2021) Circ-HIPK3 regulates YAP1 expression by sponging miR-381-3p to promote oral squamous cell carcinoma development. J. Biosci. 46, 20.   DOI
7 Blechschmidt, K., Sassen, S., Schmalfeldt, B., Schuster, T., Hofler, H. and Becker, K. F. (2008) The E-cadherin repressor Snail is associated with lower overall survival of ovarian cancer patients. Br. J. Cancer 98, 489-495.   DOI
8 Hou, Z., Peng, H., Ayyanathan, K., Yan, K. P., Langer, E. M., Longmore, G. D. and Rauscher, F. J., III (2008) The LIM protein AJUBA recruits protein arginine methyltransferase 5 to mediate SNAIL-dependent transcriptional repression. Mol. Cell. Biol. 28, 3198-3207.   DOI
9 Debnath, P., Huirem, R. S., Dutta, P. and Palchaudhuri, S. (2022) Epithelial-mesenchymal transition and its transcription factors. Biosci. Rep. 42, BSR20211754.   DOI
10 Elshami, M., Tuffaha, A., Yaseen, A., Alser, M., Al-Slaibi, I., Jabr, H., Ubaiat, S., Khader, S., Khraishi, R., Jaber, I., Abu Arafeh, Z., AlMadhoun, S., Alqattaa, A., Abd El Hadi, A., Barhoush, O., Hijazy, M., Eleyan, T., Alser, A., Abu Hziema, A., Shatat, A., Almakhtoob, F., Mohamad, B., Farhat, W., Abuamra, Y., Mousa, H., Adawi, R., Musallam, A., Abu-El-Noor, N. and Bottcher, B. (2022) Awareness of ovarian cancer risk and protective factors: a national cross-sectional study from Palestine. PLoS ONE 17, e0265452.   DOI
11 Peinado, H., Ballestar, E., Esteller, M. and Cano, A. (2004) Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol. Cell. Biol. 24, 306-319.   DOI
12 Li, X., Yang, Y. and Ashwell, J. D. (2002) TNF-RII and c-IAP1 mediate ubiquitination and degradation of TRAF2. Nature 416, 345-347.   DOI
13 Liu, C., Chen, Z., Ding, X., Qiao, Y. and Li, B. (2022) Ubiquitin-specific protease 35 (USP35) mediates cisplatin-induced apoptosis by stabilizing BIRC3 in non-small cell lung cancer. Lab. Invest. 102, 524-533.   DOI
14 Nagase, H. and Woessner, J. F., Jr. (1999) Matrix metalloproteinases. J. Biol. Chem. 274, 21491-21494.   DOI
15 Rho, S. B., Byun, H. J., Kim, B. R. and Lee, C. H. (2021a) Knockdown of LKB1 sensitizes endometrial cancer cells via AMPK activation. Biomol. Ther. (Seoul) 29, 650-657.   DOI
16 Rho, S. B., Lee, S. H., Byun, H. J., Kim, B. R. and Lee, C. H. (2020) IRF-1 inhibits angiogenic activity of HPV16 E6 oncoprotein in cervical cancer. Int. J. Mol. Sci. 21, 7622.   DOI
17 Wu, Y., Evers, B. M. and Zhou, B. P. (2009) Small C-terminal domain phosphatase enhances snail activity through dephosphorylation. J. Biol. Chem. 284, 640-648.   DOI
18 Yu, L., Kim, H. J., Park, M. K., Byun, H. J., Kim, E. J., Kim, B., Nguyen, M. T., Kim, J. H., Kang, G. J., Lee, H., Kim, S. Y., Rho, S. B. and Lee, C. H. (2021a) Ethacrynic acid, a loop diuretic, suppresses epithelial-mesenchymal transition of A549 lung cancer cells via blocking of NDP-induced WNT signaling. Biochem. Pharmacol. 183, 114339.   DOI
19 Nieto, M. A. (2002) The snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3, 155-166.   DOI
20 Peiro, S., Escriva, M., Puig, I., Barbera, M. J., Dave, N., Herranz, N., Larriba, M. J., Takkunen, M., Franci, C., Munoz, A., Virtanen, I., Baulida, J. and Garcia de Herreros, A. (2006) Snail1 transcriptional repressor binds to its own promoter and controls its expression. Nucleic Acids Res. 34, 2077-2084.   DOI
21 Rho, S. B., Lee, K. W., Lee, S. H., Byun, H. J., Kim, B. R. and Lee, C. H. (2021b) Novel anti-angiogenic and anti-tumour activities of the N-terminal domain of NOEY2 via binding to VEGFR-2 in ovarian cancer. Biomol. Ther. (Seoul) 29, 506-518.   DOI
22 Wu, Y. and Zhou, B. P. (2010) Snail: more than EMT. Cell Adh. Migr. 4, 199-203.   DOI
23 Rho, S. B., Kim, M. J., Lee, J. S., Seol, W., Motegi, H., Kim, S. and Shiba, K. (1999) Genetic dissection of protein-protein interactions in multi-tRNA synthetase complex. Proc. Natl. Acad. Sci. U.S.A. 96, 4488-4493.   DOI
24 Scheau, C., Badarau, I. A., Costache, R., Caruntu, C., Mihai, G. L., Didilescu, A. C., Constantin, C. and Neagu, M. (2019) The role of matrix metalloproteinases in the epithelial-mesenchymal transition of hepatocellular carcinoma. Anal. Cell. Pathol. 2019, 9423907.
25 Wu, Q., Zhang, Y., An, H., Sun, W., Wang, R., Liu, M. and Zhang, K. (2021a) The landscape and biological relevance of aberrant alternative splicing events in esophageal squamous cell carcinoma. Oncogene 40, 4184-4197.   DOI
26 Zender, L., Spector, M. S., Xue, W., Flemming, P., Cordon-Cardo, C., Silke, J., Fan, S.-T., Luk, J. M., Wigler, M., Hannon, G. J., Mu, D., Lucito, R., Powers, S. and Lowe, S. W. (2006) Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125, 1253-1267.   DOI
27 Kurrey, N. K., K, A. and Bapat, S. A. (2005) Snail and Slug are major determinants of ovarian cancer invasiveness at the transcription level. Gynecol. Oncol. 97, 155-165.   DOI
28 Lili, L. N., Matyunina, L. V., Walker, L., Wells, S. L., Benigno, B. B. and McDonald, J. F. (2013) Molecular profiling supports the role of epithelial-to-mesenchymal transition (EMT) in ovarian cancer metastasis. J. Ovarian Res. 6, 49.   DOI
29 Nam, M. W., Kim, C. W. and Choi, K. C. (2022) Epithelial-mesenchymal transition-inducing factors involved in the progression of lung cancers. Biomol. Ther. (Seoul) 30, 213-220.   DOI
30 Kim, H. J., Kim, B., Byun, H. J., Yu, L., Nguyen, T. M., Nguyen, T. H., Do, P. A., Kim, E. J., Cheong, K. A., Kim, K. S., Huy Phung, H., Rahman, M., Jang, J. Y., Rho, S. B., Kang, G. J., Park, M. K., Lee, H., Lee, K., Cho, J., Han, H. K., Kim, S. G., Lee, A. Y. and Lee, C. H. (2021) Resolvin D1 suppresses H2O2-induced senescence in fibroblasts by inducing autophagy through the miR-1299/ARG2/ARL1 axis. Antioxidants 10, 1924.   DOI
31 Lee, C. H. (2018) Epithelial-mesenchymal transition: initiation by cues from chronic inflammatory tumor microenvironment and termination by anti-inflammatory compounds and specialized pro-resolving lipids. Biochem. Pharmacol. 158, 261-273.   DOI
32 Lee, C. H. (2019) Reversal of epithelial-mesenchymal transition by natural anti-inflammatory and pro-resolving lipids. Cancers (Basel) 11, 1841.   DOI
33 Lin, Y., Wu, Y., Li, J., Dong, C., Ye, X., Chi, Y. I., Evers, B. M. and Zhou, B. P. (2010) The SNAG domain of Snail1 functions as a molecular hook for recruiting lysine-specific demethylase 1. EMBO J. 29, 1803-1816.   DOI
34 Mace, P. D., Linke, K., Feltham, R., Schumacher, F.-R., Smith, C. A., Vaux, D. L., Silke, J. and Day, C. L. (2008) Structures of the cIAP2 RING domain reveal conformational changes associated with ubiquitin-conjugating enzyme (E2) recruitment. J. Biol. Chem. 283, 31633-31640.   DOI
35 Yokoyama, K., Kamata, N., Fujimoto, R., Tsutsumi, S., Tomonari, M., Taki, M., Hosokawa, H. and Nagayama, M. (2003) Increased invasion and matrix metalloproteinase-2 expression by Snail-induced mesenchymal transition in squamous cell carcinomas. Int. J. Oncol. 22, 891-898.
36 Snijders, A. M., Schmidt, B. L., Fridlyand, J., Dekker, N., Pinkel, D., Jordan, R. C. and Albertson, D. G. (2005) Rare amplicons implicate frequent deregulation of cell fate specification pathways in oral squamous cell carcinoma. Oncogene 24, 4232-4242.   DOI
37 Vergara, D., Merlot, B., Lucot, J. P., Collinet, P., Vinatier, D., Fournier, I. and Salzet, M. (2010) Epithelial-mesenchymal transition in ovarian cancer. Cancer Lett. 291, 59-66.   DOI
38 Wu, S., Zang, Q., Xing, Z., Li, X., Leng, J., Liu, Y., Wang, X. and Yang, J. (2021b) A pan-cancer analysis of the BIRC gene family and its association with prognosis, tumor microenvironment, and therapeutic targets. Crit. Rev. Eukaryot. Gene Expr. 31, 35-48
39 Frazzi, R. (2021) BIRC3 and BIRC5: multi-faceted inhibitors in cancer. Cell Biosci. 11, 8.   DOI
40 Fu, P. Y., Hu, B., Ma, X. L., Yang, Z. F., Yu, M. C., Sun, H. X., Huang, A., Zhang, X., Wang, J., Hu, Z. Q., Zhou, C. H., Tang, W. G., Ning, R., Xu, Y. and Zhou, J. (2019) New insight into BIRC3: a novel prognostic indicator and a potential therapeutic target for liver cancer. J. Cell. Biochem. 120, 6035-6045.   DOI
41 Mendoza-Rodriguez, M., Romero, H. A., Fuentes-Panana, E. M., Ayala-Sumuano, J.-T. and Meza, I. (2017) IL-1β induces up-regulation of BIRC3, a gene involved in chemoresistance to doxorubicin in breast cancer cells. Cancer Lett. 390, 39-44.   DOI
42 Hou, Z., Peng, H., White, D. E., Wang, P., Lieberman, P. M., Halazonetis, T. and Rauscher, F. J. (2010) 14-3-3 binding sites in the snail protein are essential for snail-mediated transcriptional repression and epithelial-mesenchymal differentiation. Cancer Res. 70, 4385-4393.
43 Herranz, N., Pasini, D., Diaz, V. M., Franci, C., Gutierrez, A., Dave, N., Escriva, M., Hernandez-Munoz, I., Di Croce, L., Helin, K., Garcia de Herreros, A. and Peiro, S. (2008) Polycomb complex 2 is required for E-cadherin repression by the Snail1 transcription factor. Mol. Cell. Biol. 28, 4772-4781.   DOI
44 Yoneda, T., Imaizumi, K., Maeda, M., Yui, D., Manabe, T., Katayama, T., Sato, N., Gomi, F., Morihara, T., Mori, Y., Miyoshi, K., Hitomi, J., Ugawa, S., Yamada, S., Okabe, M. and Tohyama, M. (2000) Regulatory mechanisms of TRAF2-mediated signal transduction by Bcl10, a MALT lymphoma-associated protein. J. Biol. Chem. 275, 11114-11120.   DOI
45 Yu, Q., Jobin, C. and Thomas, R. M. (2021b) Implications of the microbiome in the development and treatment of pancreatic cancer: thinking outside of the box by looking inside the gut. Neoplasia 23, 246-256.   DOI
46 Yuan, H., Kajiyama, H., Ito, S., Yoshikawa, N., Hyodo, T., Asano, E., Hasegawa, H., Maeda, M., Shibata, K., Hamaguchi, M., Kikkawa, F. and Senga, T. (2013) ALX1 induces snail expression to promote epithelial-to-mesenchymal transition and invasion of ovarian cancer cells. Cancer Res. 73, 1581-1590.
47 Zheng, C., Kabaleeswaran, V., Wang, Y., Cheng, G. and Wu, H. (2010) Crystal structures of the TRAF2: cIAP2 and the TRAF1: TRAF2: cIAP2 complexes: affinity, specificity, and regulation. Mol. Cell 38, 101-113.   DOI
48 Cai, J., Gong, L., Li, G., Guo, J., Yi, X. and Wang, Z. (2021) Exosomes in ovarian cancer ascites promote epithelial-mesenchymal transition of ovarian cancer cells by delivery of miR-6780b-5p. Cell Death Dis. 12, 210.   DOI
49 Imoto, I., Tsuda, H., Hirasawa, A., Miura, M., Sakamoto, M., Hirohashi, S. and Inazawa, J. (2002) Expression of cIAP1, a target for 11q22 amplification, correlates with resistance of cervical cancers to radiotherapy. Cancer Res. 62, 4860-4866.
50 Herbert, B. S., Chanoux, R. A., Liu, Y., Baenziger, P. H., Goswami, C. P., McClintick, J. N., Edenberg, H. J., Pennington, R. E., Lipkin, S. M. and Kopelovich, L. (2010) A molecular signature of normal breast epithelial and stromal cells from Li-Fraumeni syndrome mutation carriers. Oncotarget 1, 405-422.   DOI
51 Jin, H., Yu, Y., Zhang, T., Zhou, X., Zhou, J., Jia, L., Wu, Y., Zhou, B. P. and Feng, Y. (2010) Snail is critical for tumor growth and metastasis of ovarian carcinoma. Int. J. Cancer 126, 2102-2111.   DOI
52 Bertrand, M. J., Milutinovic, S., Dickson, K. M., Ho, W. C., Boudreault, A., Durkin, J., Gillard, J. W., Jaquith, J. B., Morris, S. J. and Barker, P. A. (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30, 689-700.   DOI
53 Dai, Z., Zhu, W. G., Morrison, C. D., Brena, R. M., Smiraglia, D. J., Raval, A., Wu, Y. Z., Rush, L. J., Ross, P., Molina, J. R., Otterson, G. A. and Plass, C. (2003) A comprehensive search for DNA amplification in lung cancer identifies inhibitors of apoptosis cIAP1 and cIAP2 as candidate oncogenes. Hum. Mol. Genet. 12,791-801.   DOI
54 Dong, C., Wu, Y., Wang, Y., Wang, C., Kang, T., Rychahou, P. G., Chi, Y. I., Evers, B. M. and Zhou, B. P. (2013) Interaction with Suv39H1 is critical for Snail-mediated E-cadherin repression in breast cancer. Oncogene 32, 1351-1362.   DOI
55 Chen, P. M., Cheng, Y. W., Wu, T. C., Chen, C. Y. and Lee, H. (2015) MnSOD overexpression confers cisplatin resistance in lung adenocarcinoma via the NF-κB/Snail/Bcl-2 pathway. Free Radic. Biol. Med. 79, 127-137.   DOI
56 Hojo, N., Huisken, A. L., Wang, H., Chirshev, E., Kim, N. S., Nguyen, S. M., Campos, H., Glackin, C. A., Ioffe, Y. J. and Unternaehrer, J. J. (2018) Snail knockdown reverses stemness and inhibits tumour growth in ovarian cancer. Sci. Rep. 8, 8704.   DOI
57 Imoto, I., Yang, Z. Q., Pimkhaokham, A., Tsuda, H., Shimada, Y., Imamura, M., Ohki, M. and Inazawa, J. (2001) Identification of cIAP1 as a candidate target gene within an amplicon at 11q22 in esophageal squamous cell carcinomas. Cancer Res. 61, 6629-6634.
58 Jiang, Y., Nan, H., Shi, N., Hao, W., Dong, J. and Chen, H. (2021) Chlorogenic acid inhibits proliferation in human hepatoma cells by suppressing noncanonical NF-κB signaling pathway and triggering mitochondrial apoptosis. Mol. Biol. Rep. 48, 2351-2364.   DOI
59 Lambert, A. W. and Weinberg, R. A. (2021) Linking EMT programmes to normal and neoplastic epithelial stem cells. Nat. Rev. Cancer 21, 325-338.   DOI