Molecular biology of liver cancer stem cells

Liver Cancer

Volumn 3, Issue 2, 2014, Pages 71-84

  Oishi, Naoki ^a   Yamashita, Taro ^a   Kaneko, Shuichi ^a  

^a KANAZAWA UNIVERSITY HOSPITAL   (Japan)

Author keywords

EpCAM signaling; Hepatocellular carcinoma; Liver cancer stem cell; miR 181; Wnt signaling

Indexed keywords

ADECATUMUMAB; BETA CATENIN; CATUMAXOMAB; EPITHELIAL CELL ADHESION MOLECULE; HOMEODOMAIN PROTEIN; MICRORNA; NOTCH RECEPTOR; SAL LIKE PROTEIN 4; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN;

ANGIOGENESIS; BREAST METASTASIS; CANCER STEM CELL; CANCER THERAPY; CELL DIFFERENTIATION; CELL INVASION; CELL MIGRATION; CLINICAL TRIAL (TOPIC); EPIGENETICS; HEPATIC PROGENITOR CELL; HUMAN; HYPOXIA; IMMUNE EVASION; LIVER CANCER; LIVER CELL CARCINOMA; LIVER REGENERATION; MALIGNANT ASCITES; MOLECULAR BIOLOGY; MULTIDRUG RESISTANCE; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RADIOSENSITIVITY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SIGNAL TRANSDUCTION;

EID: 84910098336     PISSN: 22351795     EISSN: 16645553     Source Type: Journal    
DOI: 10.1159/000343863     Document Type: Review

References (61)

1. el-Serag HB: Epidemiology of hepatocellular carcinoma. Clin Liver Dis 2001;5:87-107, vi vi.
2. Russo FP, Parola M: Stem and progenitor cells in liver regeneration and repair. Cytotherapy 2011;13:135-144.
3. Michalopoulos GK: Liver regeneration. J Cell Physiol 2007;213:286-300.
4. Yamashita T, Honda M, Nakamoto Y, Baba M, Nio K, Hara Y, Zeng SS, Hayashi T, Kondo M, Takatori H, Yamashita T, Mizukoshi E, Ikeda H, Zen Y, Takamura H, Wang XW, Kaneko S: Discrete nature of EpCAM+ and CD90+ cancer stem cells in human hepatocellular carcinoma. Hepatology 2013;57:1484-1497.
5. Kitisin K, Shetty K, Mishra L, Johnson LB: Hepatocellular stem cells. Cancer Biomark 2007;3:251-262.
6. Alison MR: Liver stem cells: implications for hepatocarcinogenesis. Stem Cell Rev 2005;1:253-260.
7. Katoh M: WNT signaling pathway and stem cell signaling network. Clin Cancer Res 2007;13:4042-4045.
8. Munz M, Baeuerle PA, Gires O: The emerging role of EpCAM in cancer and stem cell signaling. Cancer Res 2009;69:5627-5629.
9. Trzpis M, McLaughlin PM, de Leij LM, Harmsen MC: Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule. Am J Pathol 2007;171:386-395.
10. Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, Kieu C, Papior P, Baeuerle PA, Munz M, Gires O: Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol 2009;11:162-171.
11. Branda M, Wands JR: Signal transduction cascades and hepatitis B and C related hepatocellular carcinoma. Hepatology 2006;43:891-902.
12. Ishizaki Y, Ikeda S, Fujimori M, Shimizu Y, Kurihara T, Itamoto T, Kikuchi A, Okajima M, Asahara T: Immunohistochemical analysis and mutational analyses of beta-catenin, Axin family and APC genes in hepatocellular carcinomas. Int J Oncol 2004;24:1077-1083.
13. Reya T, Clevers H: Wnt signalling in stem cells and cancer. Nature 2005;434:843-850.
14. Wielenga VJ, Smits R, Korinek V, Smit L, Kielman M, Fodde R, Clevers H, Pals ST: Expression of CD44 in Apc and Tcf mutant mice implies regulation by the WNT pathway. Am J Pathol 1999;154:515-523.
15. Tetsu O, McCormick F: Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999;398:422-426.
16. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW: Identification of c-MYC as a target of the APC pathway. Science 1998;281:1509-1512.
17. Münz M, Kieu C, Mack B, Schmitt B, Zeidler R, Gires O: The carcinoma-associated antigen EpCAM upregulates c-myc and induces cell proliferation. Oncogene 2004;23:5748-5758.
18. Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, Chang HY: Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2008;2:333-344.
19. Malanchi I, Huelsken J: Cancer stem cells: never Wnt away from the niche. Curr Opin Oncol 2009;21:41-46.
20. Lu TY, Lu RM, Liao MY, Yu J, Chung CH, Kao CF, Wu HC: Epithelial cell adhesion molecule regulation is associated with the maintenance of the undifferentiated phenotype of human embryonic stem cells. J Biol Chem 2010;285:8719-8732.
21. de Boer CJ, van Krieken JH, Janssen-van Rhijn CM, Litvinov SV: Expression of Ep-CAM in normal, regenerating, metaplastic, and neoplastic liver. J Pathol 1999;188:201-206.
22. Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY, Jia H, Ye Q, Qin LX, Wauthier E, Reid LM, Minato H, Honda M, Kaneko S, Tang ZY, Wang XW: EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 2009;136:1012-1024.
23. Weston CR, Davis RJ: The JNK signal transduction pathway. Curr Opin Genet Dev 2001;12:14-21.
24. Kühl M: Non-canonical Wnt signaling in Xenopus: regulation of axis formation and gastrulation. Semin Cell Dev Biol 2002;13:243-249.
25. Yuri S, Fujimura S, Nimura K, Takeda N, Toyooka Y, Fujimura Y, Aburatani H, Ura K, Koseki H, Niwa H, Nishinakamura R: Sall4 is essential for stabilization, but not for pluripotency, of embryonic stem cells by repressing aberrant trophectoderm gene expression. Stem Cells 2009;27:796-805.
26. Yong KJ, Chai L, Tenen DG: Oncofetal gene SALL4 in aggressive hepatocellular carcinoma. N Engl J Med 2013;369:1171-1172.]
27. Zeng SS, Yamashita T, Kondo M, Nio K, Hayashi T, Hara Y, Nomura Y, Yoshida M, Hayashi T, Oishi N, Ikeda H, Honda M, Kaneko S: The transcription factor SALL4 regulates stemness of EpCAM-positive hepatocellular carcinoma. J Hepatol 2014;60:127-134.
28. Tang Y, Kitisin K, Jogunoori W, Li C, Deng CX, Mueller SC, Ressom HW, Rashid A, He AR, Mendelson JS, Jessup JM, Shetty K, Zasloff M, Mishra B, Reddy EP, Johnson L, Mishra L: Progenitor/stem cells give rise to liver cancer due to aberrant TGF-beta and IL-6 signaling. Proc Natl Acad Sci USA 2008;105:2445-2450.
29. Yuan F, Zhou W, Zou C, Zhang Z, Hu H, Dai Z, Zhang Y: Expression of Oct4 in HCC and modulation to wnt/β-catenin and TGF-β signal pathways. Mol Cell Biochem 2010;343:155-162.
30. Weng AP, Aster JC: Multiple niches for Notch in cancer: context is everything. Curr Opin Genet Dev 2004;14:48-54.
31. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD: Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 2006;442:823-826.
32. Cerdan C, Bhatia M: Novel roles for Notch, Wnt and Hedgehog in hematopoesis derived from human pluripotent stem cells. Int J Dev Biol 2010;54:955-963.
33. Villavicencio EH, Walterhouse DO, Iannaccone PM: The sonic hedgehog-patched-gli pathway in human development and disease. Am J Hum Genet 2000;67:1047-1054.
34. Lum L, Beachy PA: The Hedgehog response network: sensors, switches, and routers. Science 2004;304:1755-1759.
35. Coulouarn C, Factor VM, Andersen JB, Durkin ME, Thorgeirsson SS: Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties. Oncogene 2009;28:3526-3536.
36. Pineau P, Volinia S, McJunkin K, Marchio A, Battiston C, Terris B, Mazzaferro V, Lowe SW, Croce CM, Dejean A: miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci USA 2010;107:264-269.
37. Ma S, Tang KH, Chan YP, Lee TK, Kwan PS, Castilho A, Ng I, Man K, Wong N, To KF, 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.
38. Wong QW, Lung RW, Law PT, Lai PB, Chan KY, To KF, Wong N: MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin1. Gastroenterology 2008;135:257-269.
39. Wong QW, Ching AK, Chan AW, Choy KW, To KF, Lai PB, Wong N: MiR-222 overexpression confers cell migratory advantages in hepatocellular carcinoma through enhancing AKT signaling. Clin Cancer Res 2010;16:867-875.
40. Koike H, Taniguchi H: Characteristics of hepatic stem/progenitor cells in the fetal and adult liver. J Hepatobiliary Pancreat Sci 2012;19:587-593.
41. Strahl BD, Allis CD: The language of covalent histone modifications. Nature 2000;403:41-45.
42. Stock JK, Giadrossi S, Casanova M, Brookes E, Vidal M, Koseki H, Brockdorff N, Fisher AG, Pombo A: Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol 2007;9:1428-1435.
43. Xu CR, Cole PA, Meyers DJ, Kormish J, Dent S, Zaret KS: Chromatin "prepattern" and histone modifiers in a fate choice for liver and pancreas. Science 2011;332:963-966.
44. Kubicek S, Gilbert JC, Fomina-Yadlin D, Gitlin AD, Yuan Y, Wagner FF, Holson EB, Luo T, Lewis TA, Taylor B, Gupta S, Shamji AF, Wagner BK, Clemons PA, Schreiber SL: Chromatin-targeting small molecules cause class-specific transcriptional changes in pancreatic endocrine cells. Proc Natl Acad Sci USA 2012;109:5364-5369.
45. Klonisch T, Wiechec E, Hombach-Klonisch S, Ande SR, Wesselborg S, Schulze-Osthoff K, Los M: Cancer stem cell markers in common cancers-therapeutic implications. Trends Mol Med 2008;14:450-460.
46. Dingli D, Michor F: Successful therapy must eradicate cancer stem cells. Stem Cells 2006;24:2603-2610.
47. Oishi N, Wang XW: Novel therapeutic strategies for targeting liver cancer stem cells. Int J Biol Sci 2011;7:517-535.
48. Goel S, Bauer RJ, Desai K, Bulgaru A, Iqbal T, Strachan BK, Kim G, Kaubisch A, Vanhove GF, Goldberg G, Mani S: Pharmacokinetic and safety study of subcutaneously administered weekly ING-1, a human engineere monoclonal antibody targeting human EpCAM, in patients with advanced solid tumors. Ann Oncol 2007;18:1704-1707.
49. Schmidt M, Scheulen ME, Dittrich C, Obrist P, Marschner N, Dirix L, Schmidt M, Rüttinger D, Schuler M, Reinhardt C, Awada A: An open-label, randomized phase II study of adecatumumab, a fully human anti-EpCAM antibody, as monotherapy in patients with metastatic breast cancer. Ann Oncol 2010;21:275-282.
50. Ott MG, Marmé F, Moldenhauer G, Lindhofer H, Hennig M, Spannagl R, Essing MM, Linke R, Seimetz D: Humoral response to catumaxomab correlates with clinical outcome: results of the pivotal phase II/III study in patients with malignant ascites. Int J Cancer 2012;130:2195-2203.
51. Herrmann I, Baeuerle PA, Friedrich M, Murr A, Filusch S, Rüttinger D, Majdoub MW, Sharma S, Kufer P, Raum T, Münz M: Highly efficient elimination of colorectal tumor-initiating cells by an EpCAM/CD3-bispecific antibody engaging human T cells. PLoS ONE 2010;5:e13474.
52. Yamashita T, Budhu A, Forgues M, Wang XW: Activation of hepatic stem cell marker EpCAM by Wnt-beta-catenin signaling in hepatocellular carcinoma. Cancer Res 2007;67:10831-10839.
53. Zeng G, Apte U, Cieply B, Singh S, Monga SP: siRNA-mediated beta-catenin knockdown in human hepatoma cells results in decreased growth and survival. Neoplasia 2007;9:951-959.
54. Li Y, Lu W, King TD, Liu CC, Bijur GN, Bu G: Dkk1 stabilizes Wnt co-receptor LRP6: implication for Wnt ligand-induced LRP6 down-regulation. PLoS ONE 2010;5:e11014.
55. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA, Charlat O, Wiellette E, Zhang Y, Wiessner S, Hild M, Shi X, Wilson CJ, Mickanin C, Myer V, Fazal A, Tomlinson R, Serluca F, Shao W, Cheng H, Shultz M, Rau C, Schirle M, Schlegl J, Ghidelli S, Fawell S, Lu C, Curtis D, Kirschner MW, Lengauer C, Finan PM, Tallarico JA, Bouwmeester T, Porter JA, Bauer A, Cong F: Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009;461:614-620.
56. Stanton BZ, Peng LF: Small-molecule modulators of the Sonic Hedgehog signaling pathway. Mol Biosyst 2010;6:44-54.
57. Wang Q, Huang S, Yang L, Zhao L, Yin Y, Liu Z, Chen Z, Zhang H: Down-regulation of Sonic hedgehog signaling pathway activity is involved in 5-fluorouracil-induced apoptosis and motility inhibition in Hep3B cells. Acta Biochim Biophys Sin (Shanghai) 2008;40:819-829.
58. Eichenmüller M, Gruner I, Hagl B, Häberle B, Müller-Höcker J, von Schweinitz D, Kappler R: Blocking the hedgehog pathway inhibits hepatoblastoma growth. Hepatology 2009;49:482-490.
59. Yin C, Lin Y, Zhang X, Chen YX, Zeng X, Yue HY, Hou JL, Deng X, Zhang JP, Han ZG, Xie WF: Differentiation therapy of hepatocellular carcinoma in mice with recombinant adenovirus carrying hepatocyte nuclear factor-4alpha gene. Hepatology 2008;48:1528-1539.
60. Lim R, Knight B, Patel K, McHutchison JG, Yeoh GC, Olynyk JK: Antiproliferative effects of interferon alpha on hepatic progenitor cells in vitro and in vivo. Hepatology 2006;43:1074-1083.
61. Yamashita T, Honda M, Nio K, Nakamoto Y, Yamashita T, Takamura H, Tani T, Zen Y, Kaneko S: Oncostatin m renders epithelial cell adhesion molecule-positive liver cancer stem cells sensitive to 5-Fluorouracil by inducing hepatocytic differentiation. Cancer Res 2010;70:4687-4697.