Regulatory MiR-148a-ACVR1/BMP circuit defines a cancer stem cell-like aggressive subtype of hepatocellular carcinoma

Hepatology

Volumn 61, Issue 2, 2015, Pages 574-584

  Li, Lian ^a   Liu, Yuexin ^b   Guo, Yan ^a   Liu, Ben ^a   Zhao, Yanrui ^a   Li, Pei ^a   Song, Fengju ^a   Zheng, Hong ^a   Yu, Jingpu ^c   Song, Tianqiang ^c   Niu, Ruifang ^c   Li, Qiang ^c   Wang, Xin Wei ^d   Zhang, Wei ^b   Chen, Kexin ^a  

^a KEY LABORATORY OF CANCER PREVENTION AND THERAPY   (China)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A RECEPTOR TYPE 1; BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN; INTERLEUKIN 8; MESSENGER RNA; MICRORNA; MICRORNA 148A; MOLECULAR MARKER; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; ACTIVIN RECEPTOR 1; ACVR1 PROTEIN, HUMAN; MIRN148 MICRORNA, HUMAN; WNT PROTEIN;

ACVR1 GENE; ARTICLE; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER STEM CELL; CANCER SURVIVAL; CANCER TISSUE; CD90 GENE; CONTROLLED STUDY; CS24 GENE; EPCAM GENE; FEMALE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE REPRESSION; HUMAN; HUMAN TISSUE; IL 8 GENE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; NUCLEOTIDE SEQUENCE; PERSONALIZED MEDICINE; PHENOTYPE; PRIORITY JOURNAL; RECEPTOR GENE; REGULATORY MECHANISM; RNA ANALYSIS; SIGNAL TRANSDUCTION; ADULT; AGED; ANIMAL; BAGG ALBINO MOUSE; CHINA; CLASSIFICATION; CLUSTER ANALYSIS; EPIDEMIOLOGY; HEPG2 CELL LINE; LIVER TUMOR; METABOLISM; MIDDLE AGED; MORTALITY; NUDE MOUSE; TUMOR INVASION;

ACTIVIN RECEPTORS, TYPE I; ADULT; AGED; ANIMALS; BONE MORPHOGENETIC PROTEINS; CARCINOMA, HEPATOCELLULAR; CHINA; CLUSTER ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MALE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MIDDLE AGED; NEOPLASM INVASIVENESS; WNT PROTEINS;

EID: 84921451313     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27543     Document Type: Article

References (49)

1. Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010;127:2893-2917.
2. Chen WQ, Zheng RS, Zhang SW. Liver cancer incidence and mortality in China, 2009. Chin J Cancer 2013;32:162-169.
3. Llovet JM, Bustamante J, Castells A, Vilana R, Ayuso MDC, Sala M, et al. Natural history of untreated nonsurgical hepatocellular carcinoma: rationale for the design and evaluation of therapeutic trials. Hepatology 1999;29:62-67.
4. Hoshida Y, Nijman SMB, Kobayashi M, Chan JA, Brunet J-P, Chiang DY, et al. Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma. Cancer Res 2009;69:7385-7392.
5. Boyault S, Rickman DS, de Reynies A, Balabaud C, Rebouissou S, Jeannot E, et al. Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets. Hepatology 2007;45:42-52.
6. Lee J-S, Heo J, Libbrecht L, Chu I-S, Kaposi-Novak P, Calvisi DF, et al. A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 2006;12:410-416.
7. Roessler S, Budhu A, Wang XW. Future of molecular profiling of human hepatocellular carcinoma. Future Oncol 2007;3:429-439.
8. Pineau P, Volinia S, McJunkin K, Marchio A, Battiston C, Terris B, et al. miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci U S A 2010;107:264-269.
9. Hou J, Lin L, Zhou W, Wang Z, Ding G, Dong Q, et al. Identification of miRNomes in human liver and hepatocellular carcinoma reveals miR-199a/b-3p as therapeutic target for hepatocellular carcinoma. Cancer Cell 2011;19:232-243.
10. Ji J, Yamashita T, Budhu A, Wang XW. Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology 2009;50:472-480.
11. Roessler S, Jia H-L, Budhu A, Forgues M, Ye Q-H, Lee J-S, et al. A unique metastasis gene signature enables prediction of tumor relapse in early-stage hepatocellular carcinoma patients. Cancer Res 2010;70:10202-10212.
12. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001;98:5116-5121.
13. Terris B, Cavard C, Perret C. EpCAM, a new marker for cancer stem cells in hepatocellular carcinoma. J Hepatol 2010;52:280-281.
14. Qian YW, Chen Y, Yang W, Fu J, Cao J, Ren YB, et al. p28(GANK) prevents degradation of Oct4 and promotes expansion of tumor-initiating cells in hepatocarcinogenesis. Gastroenterology 2012;142:1547-1558 e1514.
15. Liu L, Fu D, Ma Y, Shen X. The power and the promise of liver cancer stem cell markers. Stem Cells Dev 2011;20:2023-2030.
16. Lai Q, Avolio AW, Rossi M. Role of alpha-fetoprotein in selection of patients with hepatocellular carcinoma waiting for liver transplantation: must we reconsider it? Int J Biol Markers 2011;26:153-159.
17. Waugh DJJ, Wilson C. The interleukin-8 pathway in cancer. Clin Cancer Res 2008;14:6735-6741.
18. Bhattaram P, Penzo-Mendez A, Sock E, Colmenares C, Kaneko KJ, Vassilev A, et al. Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nat Commun 2010;1:9.
19. Piao LS, Hur W, Kim T-K, Hong SW, Kim SW, Choi JE, et al. CD133+ liver cancer stem cells modulate radioresistance in human hepatocellular carcinoma. Cancer Lett 2012;315:129-137.
20. Song H, Wang Q, Wen J, Liu S, Gao X, Cheng J, et al. ACVR1, a therapeutic target of fibrodysplasia ossificans progressiva, is negatively regulated by miR-148a. Int J Med Sci 2012;13:2063-2077.
21. Yamashita T, Budhu A, Forgues M, Wang XW. Activation of hepatic stem cell marker EpCAM by Wnt/beta-catein signaling in hepatocellular carcinoma. Cancer Res 2007;67:10831-10839.
22. Levy L, Neuveut C, Renard C, Charneau P, Buendia MA. Transcriptional activationof interleukin-8 by beta-catein-tcf4. J. Biol Chem 2002;277:42386-42393.
23. Meyer MB, Geotsch PD, Pike JW. VDR/RXR and TCF4/beta-catein cistromes in colonic cells of colorectal tumor origin: impact on c-FOS and c-MYC gene expression. Mol Endocrinol 2012;26:37-51.
24. Lee YS, Choi I, Ning Y, Kim NY, Khatchadourian V, Yang D, et al. Interleukin-8 and its receptor CXCR2 in the tumour microenvironment promote colon cancer growth, progression and metastasis. Br J Cancer 2012;106:1833-1841.
25. Gould SE, Day M, Jones SS, Dorai H. BMP-7 regulates chemokine, cytokine, and hemodynamic gene expression in proximal tubule cells. Kidney Int 2002;61:51-60.
26. Moylan CA, Pang H, Dellinger A, Suzuki A, Garrett ME, Guy CD, et al. Hepatic gene expression profiles differentiate presymptomatic patients with mild versus severe nonalcoholic fatty liver disease. Hepatology 2014;59:471-482.
27. Zhang Y, Baker SS, Baker RD, Zhu R, Zhu L. Systematic analysis of the gene expression in the livers of nonalcoholic steatohepatitis: implications on potential biomarkers and molecular pathological mechanism. PloS One 2012;7:e51131.
28. Lau CK, Yang ZF, Ho DW, Ng MN, Yeoh GCT, Poon RTP, et al. An Akt/hypoxia-inducible factor-1α/platelet-derived growth factor-BB autocrine loop mediates hypoxia-induced chemoresistance in liver cancer cells and tumorigenic hepatic progenitor cells. Clin Cancer Res 2009;15:3462-3471.
29. Reister S, Kordes C, Sawitza I, Haussinger D. The epigenetic regulation of stem cell factors in hepatic stellate cells. Stem Cells Dev 2011;20:1687-1699.
30. Zhang C, Wang Y, Chen H, Yang G, Wang S, Jiang M, Cong L, et al. Protective effect of the herbal medicine Ganfukang against carbon tetrachlorideinduced liver fibrosis in rats. Mol Med Rep 2013;8:954-962.
31. Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Chu PWK, et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 2008;13:153-166.
32. 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.
33. Chai S, Ma S. Clinical implications of microRNAs in liver cancer stem cells. Chin J Cancer 2013;32:419-426.
34. Shore EM, Xu M, Feldman GJ, Fenstermacher DA, Cho TJ, Choi IH, et al. A recurrent mutation in the BMP type I receptor ACVR1 causes inherited and sporadic fibrodysplasia ossificans progressiva. Nat Gen 2006;38:525-527.
35. Nakahara Y, Katagiri T, Ogata N, Haga N. ACVR1 (587T>C) mutation in a variant form of fibrodysplasia ossificans progressiva: Second report. Am J Med Genet A 2014;164:220-224.
36. Slattery ML, John EM, Torres-Mejia G, Herrick JS, Giuliano AR, Baumgartner KB, et al. Genetic variation in bone morphogenetic proteins and breast cancer risk in Hispanic and non-Hispanic white women: the Breast Cancer Health Disparities Study. Int J Cancer 2013;132:2928-2939.
37. Kevenaar ME, Themmen AP, van Kerkwijk AJ, Valkenburg O, Uitterlinden AG, de Jong FH, et al. Variants in the ACVR1 gene are associated with AMH levels in women with polycystic ovary syndrome. Hum Reprod 2009;24:241-249.
38. Kamiya N, Kaartinen VM, Mishina Y. Loss-of-function of ACVR1 in osteoblasts increases bone mass and activates canonical Wnt signaling through suppression of Wnt inhibitors SOST and DKK1. Biochem Biophys Res Commun 2011;414:326-330.
39. Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P, et al. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 2008;452:650-653.
40. Zhu A, Xia J, Zuo J, Jin S, Zhou H, Yao L, et al. MicroRNA-148a is silenced by hypermethylation and interacts with DNA methyltransferase 1 in gastric cancer. Med Oncol 2012;29:2701-2709.
41. Zhang J, Ying Z-z, Tang Z-l, Long L-q, Li K. MicroRNA-148a promotes myogenic differentiation by targeting the ROCK1 gene. J Biol Chem 2012;287:21093-21101.
42. Pan W, Zhu S, Yuan M, Cui H, Wang L, Luo X, et al. MicroRNA-21 and microRNA-148a contribute to DNA hypomethylation in lupus CD4+ T cells by directly and indirectly targeting DNA methyltransferase 1. J Immunol 2010;184:6773-6781.
43. Zheng B, Liang L, Wang C, Huang S, Cao X, Zha R, et al. MicroRNA-148a suppresses tumor cell invasion and metastasis by down-regulating ROCK1 in gastric cancer. Clin Cancer Res 2011;17:7574-7583.
44. Yuan K, Lian Z, Sun B, Clayton MM, Ng IOL, Feitelson MA. Role of miR-148a in hepatitis B associated hepatocellular carcinoma. PloS One 2012;7:e35331.
45. Budhu A, Jia H-L, Forgues M, Liu C-G, Goldstein D, Lam A, et al. Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology 2008;47:897-907.
46. Zhang JP, Zeng C, Xu L, Gong J, Fang JH, Zhuang SM. MicroRNA-148a suppresses the epithelial-mesenchymal transition and metastasis of hepatoma cells by targeting Met/Snail signaling. Oncogene 2014;33:4069-4076.
47. Yan H, Dong X, Zhong X, Ye J, Zhou Y, Yang X, et al. Inhibitions of epithelial to mesenchymal transition and cancer stem cells-like properties are involved in miR-148a-mediated anti-metastasis of hepatocellular carcinoma. Mol Carcinog 2013 [Epub ahead of print].
48. Chen Z, Ma T, Huang C, Zhang L, Xu T, Hu T, et al. MicroRNA-148a: a potential therapeutic target for cancer. Gene 2014;533:456-457.
49. Gailhouste L, Gomez-Santos L, Hagiwara K, Hatada I, Kitagawa N, Kawaharada K, et al. miR-148a plays a pivotal role in the liver by promoting the hepatospecific phenotype and suppressing the invasiveness of transformed cells. Hepatology 2013;58:1153-1165.