Epithelial-mesenchymal transition and migration of prostate cancer stem cells is driven by cancer-associated fibroblasts in an HIF-1α/β- Catenin-dependent pathway

Molecules and Cells

Volumn 36, Issue 2, 2013, Pages 138-144

  Luo, Yong ^a   Lan, Ling ^b   Jiang, Yong Guang ^a   Zhao, Jia Hui ^a   Li, Ming Chuan ^a   Wei, Neng Bao ^a   Lin, Yun Hua ^a  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b Beijing Jishuitan Hospital   (China)

Author keywords

Cancer associated fibroblast; Epithelial mesenchymal transition; Migrating cancer stem cell; Prostate cancer

Indexed keywords

BETA CATENIN; EPIDERMAL GROWTH FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; LEUKEMIA INHIBITORY FACTOR; SHORT HAIRPIN RNA; STEM CELL FACTOR; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CANCER ASSOCIATED FIBROBLAST; CANCER STEM CELL; CELL CULTURE; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FIBROBLAST; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MALE; MESENCHYME CELL; PROSTATE CANCER; PROTEIN EXPRESSION; WESTERN BLOTTING;

MUS MUSCULUS;

ANIMALS; BETA CATENIN; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; PROSTATIC NEOPLASMS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84893005680     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-013-0096-8     Document Type: Article

References (30)

1. Brabletz, T., Jung, A., Spaderna, S., Hlubek, F., and Kirchner, T. (2005). Opinion: migrating cancer stem cells -an integrated concept of malignant tumour progression. Nat. Rev. Cancer 5, 744-749.
2. Cat, B., Stuhlmann, D., Steinbrenner, H., Alili, L., Holtkötter, O., Sies, H., and Brenneisen, P. (2006). Enhancement of tumor invasion depends on transdifferentiation of skin fibroblasts mediated by reactive oxygen species. J. Cell Sci. 119, 2727-2738.
3. Chung, L.W., Baseman, A., Assikis, V., and Zhau, H.E. (2005). Molecular insights into prostate cancer progression: the missing link of tumor microenvironment. J. Urol. 173, 10-20.
4. Conley, S.J., Gheordunescu, E., Kakarala, P., Newman, B., Korkaya, H., Heath, A.N., Clouthier, S.G., and Wicha, M.S. (2012). Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc. Natl. Acad. Sci. USA 109, 2784-2789.
5. De Wever, O., and Mareel, M. (2003). Role of tissue stroma in cancer cell invasion. J. Pathol. 200, 429-447.
6. Fidler, I.J. (2003). The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat. Rev. Cancer 3, 453-458.
7. Giannoni, E., Bianchini, F., Masieri, L., Serni, S., Torre, E., Calorini, L., and Chiarugi, P. (2010). Reciprocal activation of prostate cancer cells and cancerassociated fibroblasts stimulates epithelialmesenchymal transition and cancer stemness. Cancer Res. 70, 6945-6956.
8. Giannoni, E., Bianchini, F., Calorini, L., and Chiarugi, P. (2011). Cancer associated fibroblasts exploit reactive oxygen species through a proinflammatory signature leading to epithelial mesenchymal transition and stemness. Antioxid Redox Signal. 14, 2361-2371.
9. Hermann, P.C., Huber, S.L., Herrler, T., Aicher, A., Ellwart, J.W., Guba, M., Bruns, C.J., and Heeschen, C. (2007). Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1, 313-323.
10. Hwang, R.F., Moore, T., Arumugam, T., Ramachandran, V., Amos, K.D., Rivera, A., Ji, B., Evans, D.B., and Logsdon, C.D. (2008). Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 68, 918-926.
11. Jiang, Y.G., Luo, Y., He, D.L., Li, X., Zhang, L.L., Peng, T., Li, M.C., and Lin, Y.H. (2007). Role of Wnt/beta-catenin signaling path way in epithelial-mesenchymal transition of human prostate cancer induced by hypoxia-inducible factor-1alpha. Int. J. Urol. 14, 1034-1039.
12. Joyce, J.A., and Pollard, J.W. (2009). Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252.
13. Kalluri, R. (2009). EMT: when epithelial cells decide to become mesenchymal-like cells. J. Clin. Invest. 119, 1417-1419.
14. Kalluri, R., and Zeisberg, M. (2006). Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401.
15. Kaminski, A., Hahne, J.C., Haddouti, E., Florin, A., Wellmann, A., and Wernert, N. (2006). Tumour-stroma interactions between metastatic prostate cancer cells and fibroblasts. Int. J. Mol. Med. 18, 941-950.
16. Klarmann, G.J., Hurt, E.M., Mathews, L.A., Zhang, X., Duhagon, M.A., Mistree, T., Thomas, S.B., and Farrar, W.L. (2009). Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature. Clin. Exp. Metastasis 26, 433-446.
17. Lebret, S.C., Newgreen, D.F., Thompson, E.W., and Ackland, M.L. (2007). Induction of epithelial to mesenchymal transition in PMC42-LA human breast carcinoma cells by carcinoma-associated fibroblast secreted factors. Breast Cancer Res. 9, R19.
18. Liao, C.P., Adisetiyo, H., Liang, M., and Roy-Burman, P. (2010). Cancer-associated fibroblasts enhance the gland-forming capability of prostate cancer stem cells. Cancer Res. 70, 7294-7303.
19. Liotta, L.A., and Kohn, E.C. (2001). The microenvironment of the tumour-host interface. Nature 411, 375-379.
20. Luo, Y., He, D.L., Ning, L., Shen, S.L., Li, L., Li, X., Zhau, H.E., and Chung, L.W. (2006). Over-expression of hypoxia-inducible factor-1alpha increases the invasive potency of LNCaP cells in vitro. BJU Int. 98, 1315-1319.
21. Luo, Y., Cui, X.H., Jiang, Y.G., Zhao, J.H., Zhao, L., Chen, Y.T., Li, M.C., and Lin, Y.H. (2012). Sorting and identification of cancer stem cells in human prostate cancer cell lines. Zhonghua Nan Ke Xue 18, 1062-1068.
22. Luo, Y., Cui, X.H., Jiang, Y.G., He, D.L., Zhao, J.H., Zhao, L., Chen, Y.T., Li, M.C., and Lin, Y.H. (2013). Epithelial-mesenchymal transition of prostate cancer: cancer stem cells or bulk cancer cells. Zhonghua Yi Xue Za Zhi 93, 256-260.
23. Mani, S.A., Guo, W., Liao, M.J., Eaton, E.N., Ayyanan, A., Zhou, A.Y., Brooks, M., Reinhard, F., Zhang, C.C., Shipitsin, M., et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715.
24. Silzle, T., Randolph, G.J., Kreutz, M., and Kunz-Schughart, L.A. (2004). The fibroblast: sentinel cell and local immune modulator in tumor tissue. Int. J. Cancer 108, 173-180.
25. Studebaker, A.W., Storci, G., Werbeck, J.L., Sansone, P., Sasser, A.K., Tavolari, S., Huang, T., Chan, M.W., Marini, F.C., Rosol, T.J., et al. (2008). Fibroblasts isolated from common sites of breast cancer metastasis enhance cancer cell growth rates and invasiveness in an interleukin-6-dependent manner. Cancer Res. 68, 9087-9095.
26. Sung, S,Y, Hsieh, C.L., Law, A., Zhau, H.E., Pathak, S., Multani, A.S., Lim, S., Coleman, I.M., Wu, L.C., Figg, W.D., et al. (2008). Coevolution of prostate cancer and bone stroma in threedimensional coculture: implications for cancer growth and metastasis. Cancer Res. 68, 9996-10003.
27. Thiery, J.P., Acloque, H., Huang, R.Y., and Nieto, M.A. (2009). Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890.
28. Visvader, J.E., and Lindeman, G.J. (2008). Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 8, 755-768.
29. Yang, Z.F., Ho, D.W., Ng, M.N., Lau, C.K., Yu, W.C., Ngai, P., Chu, P.W., Lam, C.T., Poon, R.T., and Fan, S.T. (2008). Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13, 153-166.
30. Zhao, J.H., Luo, Y., Jiang, Y.G., He, D.L., and Wu, C.T. (2011). Knockdown of β-Catenin through shRNA cause a reversal of EMT and metastatic phenotypes induced by HIF-1α. Cancer Invest. 29, 377-382.