Loss of Mel-18 enhances breast cancer stem cell activity and tumorigenicity through activating Notch signaling mediated by the Wnt/TCF pathway

FASEB Journal

Volumn 26, Issue 12, 2012, Pages 5002-5013

  Won, Hee Young ^a   Lee, Jeong Yeon ^a   Shin, Dong Hui ^a   Park, Ji Hye ^a   Nam, Jeong Seok ^b   Kim, Hyoung Chin ^c   Kong, Gu ^a  

^a Hanyang University   (South Korea)

^b Gachon University College of Medicine   (South Korea)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Jagged 1; Polycomb; Self renewal; Stemness

Indexed keywords

CD24 ANTIGEN; CELL SURFACE MARKER; ESA PROTEIN; HERMES ANTIGEN; JAGGED1; MEL 18 PROTEIN; NOTCH RECEPTOR; REGULATOR PROTEIN; SHORT HAIRPIN RNA; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER STEM CELL; CARCINOGENICITY; CELL COUNT; CELL POPULATION; CELL RENEWAL; CELL STRAIN MCF 7; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TARGETING; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MEDIATOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR UPREGULATION; SIDE POPULATION CELL; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR XENOGRAFT;

ANIMALS; BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOBLOTTING; MAMMARY NEOPLASMS, EXPERIMENTAL; MCF-7 CELLS; MICE; MICE, INBRED NOD; MICE, SCID; MODELS, GENETIC; NEOPLASTIC STEM CELLS; POLYCOMB REPRESSIVE COMPLEX 1; RECEPTOR, NOTCH1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIDE-POPULATION CELLS; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84870346423     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-209247     Document Type: Article

References (55)

1. Liu, S., and Wicha, M. S. (2010) Targeting breast cancer stem cells. J. Clin. Oncol. 28, 4006-4012
2. McDermott, S. P., and Wicha, M. S. (2010) Targeting breast cancer stem cells. Mol. Oncol. 4, 404-419
3. - cancer cells are similarly tumorigenic. Cancer Res. 65, 6207-6219
4. Ginestier, C., Hur, M. H., Charafe-Jauffret, E., Monville, F., Dutcher, J., Brown, M., Jacquemier, J., Viens, P., Kleer, C. G., Liu, S., Schott, A., Hayes, D., Birnbaum, D., Wicha, M. S., and Dontu, G. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1, 555-567 (Pubitemid 350056407)
5. Platet, N., Mayol, J. F., Berger, F., Herodin, F., and Wion, D. (2007) Fluctuation of the SP/non-SP phenotype in the C6 glioma cell line. FEBS Lett. 581, 1435-1440 (Pubitemid 46452620)
6. Bleau, A. M., Hambardzumyan, D., Ozawa, T., Fomchenko, E. I., Huse, J. T., Brennan, C. W., and Holland, E. C. (2009) PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 4, 226-235
7. Dubrovska, A., Kim, S., Salamone, R. J., Walker, J. R., Maira, S. M., Garcia-Echeverria, C., Schultz, P. G., and Reddy, V. A. (2009) The role of PTEN/Akt/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc. Natl. Acad. Sci. U. S. A. 106, 268-273
8. Zheng, H., Ying, H., Yan, H., Kimmelman, A. C., Hiller, D. J., Chen, A. J., Perry, S. R., Tonon, G., Chu, G. C., Ding, Z., Stommel, J. M., Dunn, K. L., Wiedemeyer, R., You, M. J., Brennan, C., Wang, Y. A., Ligon, K. L., Wong, W. H., Chin, L., and DePinho, R. A. (2008) p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 455, 1129-1133
9. Cicalese, A., Bonizzi, G., Pasi, C. E., Faretta, M., Ronzoni, S., Giulini, B., Brisken, C., Minucci, S., Di Fiore, P. P., and Pelicci, P. G. (2009) The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138, 1083-1095
10. Kakarala, M., and Wicha, M. S. (2008) Implications of the cancer stem-cell hypothesis for breast cancer prevention and therapy. J. Clin. Oncol. 26, 2813-2820
11. Pannuti, A., Foreman, K., Rizzo, P., Osipo, C., Golde, T., Osborne, B., and Miele, L. (2010) Targeting Notch to target cancer stem cells. Clin. Cancer Res. 16, 3141-3152
12. Wang, Z., Li, Y., Banerjee, S., and Sarkar, F. H. (2009) Emerging role of Notch in stem cells and cancer. Cancer Lett. 279, 8-12
13. Wang, J., Wakeman, T. P., Lathia, J. D., Hjelmeland, A. B., Wang, X. F., White, R. R., Rich, J. N., and Sullenger, B. A. (2010) Notch promotes radioresistance of glioma stem cells. Stem Cells 28, 17-28
14. Hovinga, K. E., Shimizu, F., Wang, R., Panagiotakos, G., Van Der Heijden, M., Moayedpardazi, H., Correia, A. S., Soulet, D., Major, T., Menon, J., and Tabar, V. (2010) Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate. Stem Cells 28, 1019-1029
15. Harrison, H., Farnie, G., Howell, S. J., Rock, R. E., Stylianou, S., Brennan, K. R., Bundred, N. J., and Clarke, R. B. (2010) Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res. 70, 709-718
16. Sikandar, S. S., Pate, K. T., Anderson, S., Dizon, D., Edwards, R. A., Waterman, M. L., and Lipkin, S. M. (2010) NOTCH signaling is required for formation and self-renewal of tumor-initiating cells and for repression of secretory cell differentiation in colon cancer. Cancer Res. 70, 1469-1478
17. Simon, J. A., and Kingston, R. E. (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 10, 697-708
18. Sauvageau, M., and Sauvageau, G. (2010) Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell 7, 299-313
19. Rajasekhar, V. K., and Begemann, M. (2007) Concise review: roles of polycomb group proteins in development and disease: a stem cell perspective. Stem Cells 25, 2498-2510 (Pubitemid 47582742)
20. Suva, M. L., Riggi, N., Janiszewska, M., Radovanovic, I., Provero, P., Stehle, J. C., Baumer, K., Le Bitoux, M. A., Marino, D., Cironi, L., Marquez, V. E., Clement, V., and Stamenkovic, I. (2009) EZH2 is essential for glioblastoma cancer stem cell maintenance. Cancer Res. 69, 9211-9218
21. Iliopoulos, D., Lindahl-Allen, M., Polytarchou, C., Hirsch, H. A., Tsichlis, P. N., and Struhl, K. (2010) Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol. Cell 39, 761-772
22. Chiba, T., Miyagi, S., Saraya, A., Aoki, R., Seki, A., Morita, Y., Yonemitsu, Y., Yokosuka, O., Taniguchi, H., Nakauchi, H., and Iwama, A. (2008) The polycomb gene product BMI1 contributes to the maintenance of tumor-initiating side population cells in hepatocellular carcinoma. Cancer Res. 68, 7742-7749
23. Dovey, J. S., Zacharek, S. J., Kim, C. F., and Lees, J. A. (2008) Bmi1 is critical for lung tumorigenesis and bronchioalveolar stem cell expansion. Proc. Natl. Acad. Sci. U. S. A. 105, 11857-11862
24. Abdouh, M., Facchino, S., Chatoo, W., Balasingam, V., Ferreira, J., and Bernier, G. (2009) BMI1 sustains human glioblastoma multiforme stem cell renewal. J. Neurosci. 29, 8884-8896
25. Liu, S., Dontu, G., Mantle, I. D., Patel, S., Ahn, N. S., Jackson, K. W., Suri, P., and Wicha, M. S. (2006) Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 66, 6063-6071
26. Kanno, M., Hasegawa, M., Ishida, A., Isono, K., and Taniguchi, M. (1995) mel-18, a Polycomb group-related mammalian gene, encodes a transcriptional negative regulator with tumor suppressive activity. EMBO J. 14, 5672-5678
27. Lee, J. Y., Jang, K. S., Shin, D. H., Oh, M. Y., Kim, H. J., Kim, Y., and Kong, G. (2008) Mel-18 negatively regulates INK4a/ARF-independent cell cycle progression via Akt inactivation in breast cancer. Cancer Res. 68, 4201-4209
28. Guo, W. J., Zeng, M. S., Yadav, A., Song, L. B., Guo, B. H., Band, V., and Dimri, G. P. (2007) Mel-18 acts as a tumor suppressor by repressing Bmi-1 expression and down-regulating Akt activity in breast cancer cells. Cancer Res. 67, 5083-5089 (Pubitemid 46997242)
29. Guo, B. H., Zhang, X., Zhang, H. Z., Lin, H. L., Feng, Y., Shao, J. Y., Huang, W. L., Kung, H. F., and Zeng, M. S. (2010) Low expression of Mel-18 predicts poor prognosis in patients with breast cancer. Ann. Oncol. 21, 2361-2369
30. Wang, W., Yuasa, T., Tsuchiya, N., Ma, Z., Maita, S., Narita, S., Kumazawa, T., Inoue, T., Tsuruta, H., Horikawa, Y., Saito, M., Hu, W., Ogawa, O., and Habuchi, T. (2009) The novel tumor-suppressor Mel-18 in prostate cancer: its functional polymorphism, expression and clinical significance. Int. J. Cancer 125, 2836-2843
31. Tang, B., Yoo, N., Vu, M., Mamura, M., Nam, J. S., Ooshima, A., Du, Z., Desprez, P. Y., Anver, M. R., Michalowska, A. M., Shih, J., Parks, W. T., and Wakefield, L. M. (2007) Transforming growth factor-β can suppress tumorigenesis through effects on the putative cancer stem or early progenitor cell and committed progeny in a breast cancer xenograft model. Cancer Res. 67, 8643-8652 (Pubitemid 47437440)
32. Kim, R. J., Kim, S. R., Roh, K. J., Park, S. B., Park, J. R., Kang, K. S., Kong, G., Tang, B., Yang, Y. A., Kohn, E. A., Wakefield, L. M., and Nam, J. S. (2010) Ras activation contributes to the maintenance and expansion of Sca-1pos cells in a mouse model of breast cancer. Cancer Lett. 287, 172-181
33. Iliopoulos, D., Hirsch, H. A., Wang, G., and Struhl, K. (2011) Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc. Natl. Acad. Sci. U. S. A. 108, 1397-1402
34. Yu, F., Yao, H., Zhu, P., Zhang, X., Pan, Q., Gong, C., Huang, Y., Hu, X., Su, F., Lieberman, J., and Song, E. (2007) let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131, 1109-1123 (Pubitemid 350235025)
35. Stingl, J., Eirew, P., Ricketson, I., Shackleton, M., Vaillant, F., Choi, D., Li, H. I., and Eaves, C. J. (2006) Purification and unique properties of mammary epithelial stem cells. Nature 439, 993-997 (Pubitemid 43292419)
36. Tao, L., Roberts, A. L., Dunphy, K. A., Bigelow, C., Yan, H., and Jerry, D. J. (2011) Repression of mammary stem/progenitor cells by p53 is mediated by Notch and separable from apoptotic activity. Stem Cells 29, 119-127
37. Park, J. H., Lee, J. Y., Shin, D. H., Jang, K. S., Kim, H. J., and Kong, G. (2011) Loss of Mel-18 induces tumor angiogenesis through enhancing the activity and expression of HIF-1α mediated by the PTEN/PI3K/Akt pathway. Oncogene 30, 4578-4589
38. Katoh, M. (2006) Notch ligand, JAG1, is evolutionarily conserved target of canonical WNT signaling pathway in progenitor cells. Int. J. Mol. Med. 17, 681-685
39. Pannequin, J., Bonnans, C., Delaunay, N., Ryan, J., Bourgaux, J. F., Joubert, D., and Hollande, F. (2009) The wnt target jagged-1 mediates the activation of notch signaling by progastrin in human colorectal cancer cells. Cancer Res. 69, 6065-6073
40. Estrach, S., Ambler, C. A., Lo Celso, C., Hozumi, K., and Watt, F. M. (2006) Jagged 1 is a β-catenin target gene required for ectopic hair follicle formation in adult epidermis. Development 133, 4427-4438 (Pubitemid 46017818)
41. Korkaya, H., Paulson, A., Charafe-Jauffret, E., Ginestier, C., Brown, M., Dutcher, J., Clouthier, S. G., and Wicha, M. S. (2009) Regulation of mammary stem/progenitor cells by PTEN/Akt/β-catenin signaling. PLoS Biol. 7, e1000121
42. DiMeo, T. A., Anderson, K., Phadke, P., Fan, C., Perou, C. M., Naber, S., and Kuperwasser, C. (2009) A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res. 69, 5364-5373
43. Zeng, Y. A., and Nusse, R. (2010) Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 6, 568-577
44. Liu, S., Dontu, G., and Wicha, M. S. (2005) Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res. 7, 86-95 (Pubitemid 40704127)
45. Dontu, G., Jackson, K. W., McNicholas, E., Kawamura, M. J., Abdallah, W. M., and Wicha, M. S. (2004) Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res. 6, R605-615
46. Cui, H., Ma, J., Ding, J., Li, T., Alam, G., and Ding, H. F. (2006) Bmi-1 regulates the differentiation and clonogenic self-renewal of I-type neuroblastoma cells in a concentration-dependent manner. J. Biol. Chem. 281, 34696-34704 (Pubitemid 46036675)
47. Zhang, X. W., Sheng, Y. P., Li, Q., Qin, W., Lu, Y. W., Cheng, Y. F., Liu, B. Y., Zhang, F. C., Li, J., Dimri, G. P., and Guo, W. J. (2010) BMI1 and Mel-18 oppositely regulate carcinogenesis and progression of gastric cancer. Mol. Cancer 9, 40
48. Kajiume, T., Ohno, N., Sera, Y., Kawahara, Y., Yuge, L., and Kobayashi, M. (2009) Reciprocal expression of Bmi1 and Mel-18 is associated with functioning of primitive hematopoietic cells. Exp Hematol. 37, 857,e2-866.e2
49. Fan, X., Khaki, L., Zhu, T. S., Soules, M. E., Talsma, C. E., Gul, N., Koh, C., Zhang, J., Li, Y. M., Maciaczyk, J., Nikkhah, G., Dimeco, F., Piccirillo, S., Vescovi, A. L., and Eberhart, C. G. (2010) NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 28, 5-16
50. Nefedova, Y., Sullivan, D. M., Bolick, S. C., Dalton, W. S., and Gabrilovich, D. I. (2008) Inhibition of Notch signaling induces apoptosis of myeloma cells and enhances sensitivity to chemotherapy. Blood 111, 2220-2229 (Pubitemid 351451536)
51. Santagata, S., Demichelis, F., Riva, A., Varambally, S., Hofer, M. D., Kutok, J. L., Kim, R., Tang, J., Montie, J. E., Chinnaiyan, A. M., Rubin, M. A., and Aster, J. C. (2004) JAGGED1 expression is associated with prostate cancer metastasis and recurrence. Cancer Res. 64, 6854-6857 (Pubitemid 39330990)
52. Lin, J. T., Chen, M. K., Yeh, K. T., Chang, C. S., Chang, T. H., Lin, C. Y., Wu, Y. C., Su, B. W., Lee, K. D., and Chang, P. J. (2010) Association of high levels of Jagged-1 and Notch-1 expression with poor prognosis in head and neck cancer. Ann. Surg. Oncol. 17, 2976-2983
53. Reedijk, M., Odorcic, S., Chang, L., Zhang, H., Miller, N., McCready, D. R., Lockwood, G., and Egan, S. E. (2005) High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res. 65, 8530-8537 (Pubitemid 41330622)
54. Reedijk, M., Pinnaduwage, D., Dickson, B. C., Mulligan, A. M., Zhang, H., Bull, S. B., O'Malley, F. P., Egan, S. E., and Andrulis, I. L. (2008) JAG1 expression is associated with a basal phenotype and recurrence in lymph node-negative breast cancer. Breast Cancer Res. Treat. 111, 439-448
55. Park, J. T., Chen, X., Trope, C. G., Davidson, B., Shih Ie, M., and Wang, T. L. (2010) Notch3 overexpression is related to the recurrence of ovarian cancer and confers resistance to carboplatin. Am. J. Pathol. 177, 1087-1094