BMP4 administration induces differentiation of CD133+ hepatic cancer stem cells blocking their contributions to hepatocellular carcinoma

Cancer Research

Volumn 72, Issue 16, 2012, Pages 4276-4285

  Zhang, Lixing ^a   Sun, Hefen ^a   Zhao, Fangyu ^a   Lu, Ping ^a   Ge, Chao ^a   Li, Hong ^a   Hou, Helei ^a   Yan, Mingxia ^a   Chen, Taoyang ^b   Jiang, Guoping ^c   Xie, Haiyang ^c   Cui, Ying ^d   Huang, Xiaowu ^e   Fan, Jia ^e   Yao, Ming ^a   Li, Jinjun ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Qi Dong Liver Cancer Institute   (China)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d Guangxi Cancer Institute   (China)

^e FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; CYTOKERATIN 18; CYTOKERATIN 19; DOXORUBICIN; MITOGEN ACTIVATED PROTEIN KINASE 1; SMAD1 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; SMAD6 PROTEIN; SMAD8 PROTEIN; VINCRISTINE;

ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER STEM CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

ANTIGENS, CD; BONE MORPHOGENETIC PROTEIN 4; CARCINOMA, HEPATOCELLULAR; CELL DIFFERENTIATION; GLYCOPROTEINS; HUMANS; LIVER NEOPLASMS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASTIC STEM CELLS; PEPTIDES; PHOSPHORYLATION; SMAD6 PROTEIN;

EID: 84865133667     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-1013     Document Type: Article

References (43)

1. Ye QH, Qin LX, Forgues M, He P, Kim JW, Peng AC, et al. Predicting hepatitis B virus-positive metastatic hepatocellular carcinomas using gene expression profiling and supervised machine learning. Nat Med 2003;9:416-23. (Pubitemid 36460075)
2. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009;138:645-59.
3. Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, Iwama A, et al. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology 2006;44:240-51. (Pubitemid 44049156)
4. Cao L, Zhou Y, Zhai B, Liao J, Xu W, Zhang R, et al. Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines. BMC Gastroenterol 2011;11:71.
5. Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY, et al. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 2009;136:1012-24.
6. Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, et al. Significance of CD90 +cancer stem cells in human liver cancer. Cancer Cell 2008;13:153-66. (Pubitemid 351163165)
7. Yamashita T, Forgues M, Wang W, Kim JW, Ye Q, Jia H, et al. EpCAM and alpha-fetoprotein expression defines novel prognostic subtypes of hepatocellular carcinoma. Cancer Res 2008;68:1451-61. (Pubitemid 351346853)
8. Lee TK, Castilho A, Cheung VC, Tang KH, Ma S, Ng IO. CD24(+) liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation. Cell Stem Cell 2011;9:50-63.
9. Yin S, Li J, Hu C, Chen X, Yao M, Yan M, et al. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer 2007;120:1444-50. (Pubitemid 46355378)
10. Zhu Z, Hao X, Yan M, Yao M, Ge C, Gu J, et al. Cancer stem/progenitor cells are highly enriched in CD133+CD44+ population in hepatocellular carcinoma. Int J Cancer 2010;126:2067-78.
11. Si-Tayeb K, Lemaigre FP, Duncan SA. Organogenesis and development of the liver. Dev Cell 2010;18:175-89.
12. Chen D, Ji X, Harris MA, Feng JQ, Karsenty G, Celeste AJ, et al. Differential roles for bone morphogenetic protein (BMP) receptor type IB and IA in differentiation and specification of mesenchymal precursor cells to osteoblast and adipocyte lineages. J Cell Biol 1998;142:295-305. (Pubitemid 28341159)
13. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003;425:577-84. (Pubitemid 37280136)
14. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, et al. Smad6 inhibits signalling by the TGF-beta superfamily. Nature 1997;389:622-6. (Pubitemid 27446182)
15. Lombardo Y, Scopelliti A, Cammareri P, Todaro M, Iovino F, Ricci-Vitiani L, et al. Bone morphogenetic protein 4 induces differentiation of colorectal cancer stem cells and increases their response to chemotherapy in mice. Gastroenterology 2011;140:297-309.
16. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006;444:761-5. (Pubitemid 44949605)
17. Li F, Liu P, Liu C, Xiang D, Deng L, Li W, et al. Hepatoblast-like progenitor cells derived from embryonic stem cells can repopulate livers of mice. Gastroenterology 2010;139:2158-69. e8.
18. Lemaigre FP. Mechanisms of liver development: concepts for understanding liver disorders and design of novel therapies. Gastroenterology 2009;137:62-79.
19. MaS, Tang KH, ChanYP, Lee TK, Kwan PS, Castilho A, et al. miR-130b Promotes CD133(+) liver tumor-initiating cell growth and self-renewal via tumor protein 53-induced nuclear protein 1. Cell Stem Cell 2010;7:694-707.
20. Kim H, Choi GH, Na DC, Ahn EY, Kim GI, Lee JE, et al. Human hepatocellular carcinomas with "Stemness"-related marker expression: keratin 19 expression and a poor prognosis. Hepatology 2011;54:1707-17.
21. Fiegel HC, Park JJ, Lioznov MV, Martin A, Jaeschke-Melli S, Kaufmann PM, et al. Characterization of cell types during rat liver development. Hepatology 2003;37:148-54. (Pubitemid 36042155)
22. HuC, Li H, Li J, Zhu Z, Yin S,Hao X, et al. Analysis ofABCG2expression and side population identifies intrinsic drug efflux in the HCC cell line MHCC-97L and its modulation by Akt signaling. Carcinogenesis 2008;29:2289-97.
23. Chiu CY, Kuo KK, Kuo TL, Lee KT, Cheng KH. The activation of MEK/ERK signaling pathway by bone morphogenetic protein 4 to increase hepatocellular carcinoma cell proliferation and migration. Mol Cancer Res 2012;10:415-27.
24. Lee YC, Cheng CJ, Bilen MA, Lu JF, Satcher RL, Yu-Lee LY, et al. BMP4 promotes prostate tumor growth in bone through osteogenesis. Cancer Res 2011;71:5194-203.
25. Javelaud D, Mauviel A. Crosstalk mechanisms between the mitogen-activated protein kinase pathways and Smad signaling downstream of TGF-beta: implications for carcinogenesis.Oncogene2005;24:5742-50. (Pubitemid 43086134)
26. Chou WC, Dang CV. Acute promyelocytic leukemia: recent advances in therapy and molecular basis of response to arsenic therapies. Curr Opin Hematol 2005;12:1-6. (Pubitemid 40189232)
27. Fan J, Shen H, Dai Q, Minuk GY, Burzynski FJ, Gong Y. Bone morphogenetic protein-4 induced rat hepatic progenitor cell (WB-F344 cell) differentiationtowardhepatocytelineage. JCellPhysiol2009;220:72-81.
28. Vicente Lopez MA, Vazquez Garcia MN, Entrena A, Olmedillas Lopez S, Garcia-Arranz M, Garcia-Olmo D, et al. Low doses of bone morphogenetic protein 4 increase the survival of human adipose-derived stem cells maintaining their stemness and multipotency. Stem Cells Dev 2010;20:1011-9.
29. Langenfeld EM, Calvano SE, Abou-Nukta F, Lowry SF, Amenta P, Langenfeld J. The mature bone morphogenetic protein-2 is aberrantly expressed in non-small cell lung carcinomas and stimulates tumor growth of A549 cells. Carcinogenesis 2003;24:1445-54. (Pubitemid 37160834)
30. Buckley S, Shi W, Driscoll B, Ferrario A, Anderson K, Warburton D. BMP4 signaling induces senescence and modulates the oncogenic phenotype of A549 lung adenocarcinomacells.AmJ Physiol Lung Cell Mol Physiol 2004;286:L81-6. (Pubitemid 38055861)
31. Singh A, Morris RJ. The Yin and Yang of bone morphogenetic proteins in cancer. Cytokine Growth Factor Rev 2010;21:299-313.
32. Maegdefrau U, Amann T, Winklmeier A, Braig S, Schubert T, Weiss TS, et al. Bone morphogenetic protein 4 is induced in hepatocellular carcinoma by hypoxia and promotes tumour progression. J Pathol 2009;218:520-9.
33. Maegdefrau U, Bosserhoff AK.BMPactivated Smad signaling strongly promotes migration and invasion of hepatocellular carcinoma cells. Exp Mol Pathol 2011;92:74-81.
34. Guo X, Xiong L, Zou L, Zhao J. Upregulation of bone morphogenetic protein 4 is associated with poor prognosis in patients with hepatocellular carcinoma. Pathol Oncol Res 2012;18:635-40.
35. Mangone FR, Walder F, Maistro S, Pasini FS, Lehn CN, Carvalho MB, et al. Smad2 and Smad6 as predictors of overall survival in oral squamous cell carcinoma patients. Mol Cancer 2010;9:106.
36. Burdon T, Stracey C, Chambers I, Nichols J, Smith A. Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev Biol 1999;210:30-43. (Pubitemid 29275085)
37. Li J, Wang G, Wang C, Zhao Y, Zhang H, Tan Z, et al. MEK/ERK signaling contributes to the maintenance of human embryonic stem cell self-renewal. Differentiation 2007;75:299-307. (Pubitemid 46434953)
38. Ding W, Mouzaki M, You H, Laird JC, Mato J, Lu SC, et al. CD133+liver cancer stem cells from methionine adenosyl transferase 1A-deficient mice demonstrate resistance to transforming growth factor (TGF)-beta-induced apoptosis. Hepatology 2009;49:1277-86.
39. Tabu K, Kimura T, Sasai K, Wang L, Bizen N, Nishihara H, et al. Analysis of an alternative human CD133 promoter reveals the implication of Ras/ERK pathway in tumor stem-like hallmarks. Mol Cancer 2010;9:39.
40. Hayashida T, Decaestecker M, Schnaper HW. Cross-talk between ERK MAP kinase and Smad signaling pathways enhances TGF-beta-dependent responses in human mesangial cells. FASEB J 2003;17:1576-8.
41. Watanabe H, de Caestecker MP, Yamada Y. Transcriptional cross-talk between Smad, ERK1/2, and p38 mitogen-activated protein kinase pathways regulates transforming growth factor-beta-induced aggrecan gene expression in chondrogenic ATDC5 cells. J Biol Chem 2001;276:14466-73.
42. Zhou Q, Heinke J, Vargas A, Winnik S, Krauss T, Bode C, et al. ERK signaling is a central regulator for BMP-4 dependent capillary sprouting. Cardiovasc Res 2007;76:390-9. (Pubitemid 350007461)
43. Li Z, Fei T, Zhang J, Zhu G, Wang L, Lu D, et al. BMP4 signaling acts via dual-specificity phosphatase 9 to control ERK activity in mouse embryonic stem cells. Cell Stem Cell 2012;10:171-82.