Survivin promotes the invasion of human colon carcinoma cells by regulating the expression of MMP‑7

Gao,Fei; Zhang,Yuqin; Yang,Feng; Wang,Peng; Wang,Wenjun; Su,Yan; Luo,Weiren

doi:10.3892/mmr.2014.1897

Survivin promotes the invasion of human colon carcinoma cells by regulating the expression of MMP‑7

Authors:
- Fei Gao
- Yuqin Zhang
- Feng Yang
- Peng Wang
- Wenjun Wang
- Yan Su
- Weiren Luo
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Affiliations: Cancer Research Institute, Department of Radiotherapy of Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong 510515, P.R. China, Secondary Clinical College, Guangdong Medical College, Dongguan, Guangdong 523808, P.R. China, Department of Neurosurgery, Guangdong General Hospital, Guangdong Academy of Medical Sciences, Guangzhou, Guangdong 510080, P.R. China
Published online on: January 14, 2014 https://doi.org/10.3892/mmr.2014.1897
Pages: 825-830

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Abstract

Increased expression levels of survivin are crucial for invasion activity in several types of human cancer, including colon carcinoma. However, the molecular mechanisms whereby survivin regulates cancer invasion have not been completely elucidated. To the best of our knowledge, this study is the first to investigate the role of matrix metalloprotease‑7 (MMP‑7) in cell invasion that is induced by survivin by using in vitro assays, including western blot, immunofluorescence and qPCR analyses. The results demonstrated that the ectopic expression of survivin significantly promoted the invasive activity of colon carcinoma cells (SW620 and HCT‑116) and resulted in increased levels of MMP‑7 activation. By contrast, the small interfering RNA (siRNA)‑based knockdown of survivin markedly reduced cell migration and led to a dose‑dependent decrease in MMP‑7 expression levels. Compared with the controls, knockdown of MMP‑7 by siRNA in colon carcinoma cells led to reduced invasion ability, whereas no obvious changes were observed when MMP‑7 expression was silenced in survivin‑overexpressing colon carcinoma cells. These findings demonstrate that MMP‑7 is crucial for survivin‑mediated invasiveness, suggesting that the survivin‑mediated MMP‑7 signaling pathway is a potential therapeutic target for the treatment of colon carcinoma.

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1	Mita AC, Mita MM, Nawrocki ST and Giles FJ: Survivin: key regulator of mitosis and apoptosis and novel target for cancer therapeutics. Clin Cancer Res. 14:5000–5005. 2008. View Article : Google Scholar : PubMed/NCBI
2	McKenzie JA, Liu T, Goodson AG and Grossman D: Survivin enhances motility of melanoma cells by supporting Akt activation and α5 integrin upregulation. Cancer Res. 70:7927–7937. 2010.PubMed/NCBI
3	Zhang M, Coen JJ, Suzuki Y, et al: Survivin is a potential mediator of prostate cancer metastasis. Int J Radiat Oncol Biol Phys. 78:1095–1103. 2010. View Article : Google Scholar : PubMed/NCBI
4	Abdraboh ME, Gaur RL, Hollenbach AD, Sandquist D, Raj MH and Ouhtit A: Survivin is a novel target of CD44-promoted breast tumor invasion. Am J Pathol. 179:555–563. 2011. View Article : Google Scholar : PubMed/NCBI
5	Zhonghong L, Lianjie L, Changqing Z, Ying H, Yu J and Yan L: The influence of survivin shRNA on the cell cycle and the invasion of SW480 cells of colorectal carcinoma. J Exp Clin Cancer Res. 27:202008. View Article : Google Scholar : PubMed/NCBI
6	Chu XY, Chen LB, Wang JH, et al: Overexpression of survivin is correlated with increased invasion and metastasis of colorectal cancer. J Surg Oncol. 105:520–528. 2012. View Article : Google Scholar : PubMed/NCBI
7	Chen P and Parks WC: Role of matrix metalloproteinases in epithelial migration. J Cell Biochem. 108:1233–1243. 2009. View Article : Google Scholar : PubMed/NCBI
8	Ii M, Yamamoto H, Adachi Y, Maruyama Y and Shinomura Y: Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Exp Biol Med (Maywood). 231:20–27. 2006.PubMed/NCBI
9	Wang FQ, So J, Reierstad S and Fishman DA: Matrilysin (MMP-7) promotes invasion of ovarian cancer cells by activation of progelatinase. Int J Cancer. 114:19–31. 2005. View Article : Google Scholar : PubMed/NCBI
10	Lynch CC, Hikosaka A, Acuff HB, et al: MMP-7 promotes prostate cancer-induced osteolysis via the solubilization of RANKL. Cancer Cell. 7:485–496. 2005. View Article : Google Scholar : PubMed/NCBI
11	Shi M, Liu D, Duan H, et al: Catecholamine up-regulates MMP-7 expression by activating AP-1 and STAT3 in gastric cancer. Mol Cancer. 9:2692010.PubMed/NCBI
12	Sizemore ST and Keri RA: The forkhead box transcription factor FOXC1 promotes breast cancer invasion by inducing matrix metalloprotease 7 (MMP7) expression. J Biol Chem. 287:24631–24640. 2012. View Article : Google Scholar : PubMed/NCBI
13	Miyamoto S, Yano K, Sugimoto S, et al: Matrix metalloproteinase-7 facilitates insulin-like growth factor bioavailability through its proteinase activity on insulin-like growth factor binding protein 3. Cancer Res. 64:665–671. 2004. View Article : Google Scholar : PubMed/NCBI
14	Ho BY, Wu YM, Chang KJ and Pan TM: Dimerumic acid inhibits SW620 cell invasion by attenuating H₂O₂-mediated MMP-7 expression via JNK/C-Jun and ERK/C-Fos activation in an AP-1-dependent manner. Int J Biol Sci. 7:869–880. 2011.PubMed/NCBI
15	Lee SK, Han YM, Yun J, et al: Phosphatase of regenerating liver-3 promotes migration and invasion by upregulating matrix metalloproteinases-7 in human colorectal cancer cells. Int J Cancer. 131:E190–E203. 2012. View Article : Google Scholar : PubMed/NCBI
16	Wang WS, Chen PM, Wang HS, Liang WY and Su Y: Matrix metalloproteinase-7 increases resistance to Fas-mediated apoptosis and is a poor prognostic factor of patients with colorectal carcinoma. Carcinogenesis. 27:1113–1120. 2006. View Article : Google Scholar : PubMed/NCBI
17	Koskensalo S, Louhimo J, Nordling S, Hagström J and Haglund C: MMP-7 as a prognostic marker in colorectal cancer. Tumour Biol. 32:259–264. 2011. View Article : Google Scholar : PubMed/NCBI
18	Fang YJ, Lu ZH, Wang GQ, et al: Elevated expressions of MMP7, TROP2, and survivin are associated with survival, disease recurrence, and liver metastasis of colon cancer. Int J Colorectal Dis. 24:875–884. 2009. View Article : Google Scholar : PubMed/NCBI
19	Wang GQ, Lu ZH, Fang YJ, Chen G, Zhou ZW, Pan ZZ and Wan DS: Expression and clinical significance of survivin and matrix metalloproteinase-7 in colon cancer. Ai Zheng. 28:945–949. 2009.(In Chinese).
20	Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin. 61:69–90. 2011. View Article : Google Scholar
21	Kelley RK, Wang G and Venook AP: Biomarker use in colorectal cancer therapy. J Natl Compr Canc Netw. 9:1293–1302. 2011.PubMed/NCBI
22	Altieri DC: Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer. 8:61–70. 2008. View Article : Google Scholar : PubMed/NCBI
23	Erkanli S, Bolat F, Kayaselcuk F, Demirhan B and Kuscu E: COX-2 and survivin are overexpressed and positively correlated in endometrial carcinoma. Gynecol Oncol. 104:320–325. 2007. View Article : Google Scholar : PubMed/NCBI
24	Pennati M, Folini M and Zaffaroni N: Targeting survivin in cancer therapy: fulfilled promises and open questions. Carcinogenesis. 28:1133–1139. 2007. View Article : Google Scholar : PubMed/NCBI
25	Wu JB, Nan QZ, Ma GF, et al: Short hairpin RNA-mediated survivin gene silencing inhibits invasion and metastasis of human colon carcinoma cell line SW480 in vitro. Nan Fang Yi Ke Da Xue Xue Bao. 27:951–954. 2007.(In Chinese).
26	Church DN and Talbot DC: Survivin in solid tumors: rationale for development of inhibitors. Curr Oncol Rep. 14:120–128. 2012. View Article : Google Scholar : PubMed/NCBI
27	Altieri DC: Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene. 22:8581–8589. 2003. View Article : Google Scholar : PubMed/NCBI
28	Kelly RJ, Lopez-Chavez A, Citrin D, Janik JE and Morris JC: Impacting tumor cell-fate by targeting the inhibitor of apoptosis protein survivin. Mol Cancer. 10:352011. View Article : Google Scholar : PubMed/NCBI