Human hepatic cancer stem cells are characterized by common stemness traits and diverse oncogenic pathways

Hepatology

Volumn 54, Issue 3, 2011, Pages 1031-1042

  Marquardt, Jens U ^a   Raggi, Chiara ^a   Andersen, Jesper B ^a   Seo, Daekwan ^a   Avital, Itzhak ^b   Geller, David ^c   Lee, Yun Han ^a   Kitade, Mitsuteru ^a   Holczbauer, Agnes ^a   Gillen, Matthew C ^a   Conner, Elizabeth A ^a   Factor, Valentina M ^a   Thorgeirsson, Snorri S ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAMTS1 PROTEIN; AXIN 2 PROTEIN; BETA CATENIN; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; CYTOKERATIN 19; DNA METHYLTRANSFERASE 1; EDN1 PROTEIN; EP400 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPITHELIAL CELL ADHESION MOLECULE; FRACTALKINE; HEPATOCYTE NUCLEAR FACTOR 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; STEM CELL FACTOR; TISSUE INHIBITOR OF METALLOPROTEINASE 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX4; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTOME; TUMOR MARKER; UNCLASSIFIED DRUG; WNT PROTEIN; ZEBULARINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CANCER SURVIVAL; CARCINOGENICITY; CELL ISOLATION; CELL RENEWAL; COLON CANCER; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC REGULATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LUNG ADENOCARCINOMA; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PANCREAS CANCER; PREDICTION; PRIORITY JOURNAL; RNA ANALYSIS; SCID MOUSE; SIDE POPULATION CELL; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; CELL LINE, TUMOR; CYTIDINE; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; HUMANS; LIVER NEOPLASMS; MICE; NEOPLASTIC STEM CELLS;

EID: 80052031109     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24454     Document Type: Article

References (39)

1. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
2. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66: 9339-9344.
3. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003; 100: 3983-3988.
4. 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: 240-251.
5. Curtis SJ, Sinkevicius KW, Li D, Lau AN, Roach RR, Zamponi R, et al. Primary tumor genotype is an important determinant in identification of lung cancer propagating cells. Cell Stem Cell 2010; 7: 127-133.
6. Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007; 132: 2542-2556.
7. 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: 1012-1024.
8. 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: 153-166.
9. Potgens AJ, Schmitz U, Kaufmann P, Frank HG. Monoclonal antibody CD133-2 (AC141) against hematopoietic stem cell antigen CD133 shows crossreactivity with cytokeratin 18. J Histochem Cytochem 2002; 50: 1131-1134.
10. Taussig DC, Miraki-Moud F, Anjos-Afonso F, Pearce DJ, Allen K, Ridler C, et al. Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood 2008; 112: 568-575.
11. Sullivan JP, Minna JD. Tumor oncogenotypes and lung cancer stem cell identity. Cell Stem Cell 2010; 7: 2-4.
12. Haraguchi N, Utsunomiya T, Inoue H, Tanaka F, Mimori K, Barnard GF, et al. Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 2006; 24: 506-513.
13. Feinberg AP, Ohlsson R, Henikoff S. The epigenetic progenitor origin of human cancer. Nat Rev Genet 2006; 7: 21-33.
14. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128: 683-692.
15. Andersen JB, Factor VM, Marquardt JU, Raggi C, Lee YH, Seo D, et al. An integrated genomic and epigenomic approach predicts therapeutic response to zebularine in human liver cancer. Sci Transl Med 2010; 2: 54ra77.
16. Frank NY, Schatton T, Frank MH. The therapeutic promise of the cancer stem cell concept. J Clin Invest 2010; 120: 41-50.
17. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med 2006; 355: 1253-1261.
18. Kakarala M, Wicha MS. Implications of the cancer stem-cell hypothesis for breast cancer prevention and therapy. J Clin Oncol 2008; 26: 2813-2820.
19. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996; 183: 1797-1806.
20. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature 2008; 456: 593-598.
21. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004; 6: 1-6.
22. Cheng JC, Yoo CB, Weisenberger DJ, Chuang J, Wozniak C, Liang G, et al. Preferential response of cancer cells to zebularine. Cancer Cell 2004; 6: 151-158.
23. 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.
24. Lee JS, Heo J, Libbrecht L, Chu IS, 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.
25. Ikushima H, Todo T, Ino Y, Takahashi M, Miyazawa K, Miyazono K. Autocrine TGF-beta signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors. Cell Stem Cell 2009; 5: 504-514.
26. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006; 441: 431-436.
27. Gardiner-Garden M, Frommer M. CpG islands in vertebrate genomes. J Mol Biol 1987; 196: 261-282.
28. Antequera F. Structure, function and evolution of CpG island promoters. Cell Mol Life Sci 2003; 60: 1647-1658.
29. Lee JS, Chu IS, Heo J, Calvisi DF, Sun Z, Roskams T, et al. Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling. HEPATOLOGY 2004; 40: 667-676.
30. Hu Z, Fan C, Oh DS, Marron JS, He X, Qaqish BF, et al. The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 2006; 7: 96.
31. Whitfield ML, Sherlock G, Saldanha AJ, Murray JI, Ball CA, Alexander KE, et al. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol Biol Cell 2002; 13: 1977-2000.
32. Garber ME, Troyanskaya OG, Schluens K, Petersen S, Thaesler Z, Pacyna-Gengelbach M, et al. Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci U S A 2001; 98: 13784-13789.
33. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40: 499-507.
34. Kaposi-Novak P, Libbrecht L, Woo HG, Lee YH, Sears NC, Conner EA, et al. Central role of c-Myc during malignant conversion in human hepatocarcinogenesis. Cancer Res 2009; 69: 2775-2782.
35. Llovet JM, Bruix J. Molecular targeted therapies in hepatocellular carcinoma. HEPATOLOGY 2008; 48: 1312-1327.
36. Yeatman TJ. A renaissance for SRC. Nat Rev Cancer 2004; 4: 470-480.
37. Alison MR. Liver stem cells: implications for hepatocarcinogenesis. Stem Cell Rev 2005; 1: 253-260.
38. Yang W, Yan HX, Chen L, Liu Q, He YQ, Yu LX, et al. Wnt/beta-catenin signaling contributes to activation of normal and tumorigenic liver progenitor cells. Cancer Res 2008; 68: 4287-4295.
39. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008; 359: 378-390.