Side population cell fractions from hepatocellular carcinoma cell lines increased with tumor dedifferentiation, but lack characteristic features of cancer stem cells

Journal of Gastroenterology and Hepatology (Australia)

Volumn 29, Issue 5, 2014, Pages 1092-1101

  Nakayama, Masamichi ^a   Ogasawara, Sachiko ^a   Akiba, Jun ^a   Ueda, Kosuke ^a   Koura, Keiko ^a   Todoroki, Keita ^a   Kinoshita, Hisafumi ^a   Yano, Hirohisa ^a  

^a KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cancer stem cells; Dedifferentiation; Side population cells

Indexed keywords

BMI1 PROTEIN; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; CISPLATIN; CYTOCHROME P450 3A4; EPITHELIAL CELL ADHESION MOLECULE; FLUOROURACIL; HERMES ANTIGEN; MICROSOMAL AMINOPEPTIDASE; PEGINTERFERON ALPHA2B; THY 1 ANTIGEN; TRANSCRIPTION FACTOR NANOG; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CANCER STEM CELL; CARCINOGENICITY; CARCINOMA CELL; CELL COUNT; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL DEDIFFERENTIATION; CELL FRACTIONATION; CELL GROWTH; CELL ISOLATION; CELL PROLIFERATION; CELL SELECTION; CELL VIABILITY; COLONY FORMING UNIT; CONTROLLED STUDY; DRUG EXPOSURE; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MICROARRAY ANALYSIS; MOUSE; MTT ASSAY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIDE POPULATION CELL; CELL DIFFERENTIATION; CELL SEPARATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIVER TUMOR; METABOLISM; PATHOLOGY; PROCEDURES; TUMOR CELL LINE;

ANTIGENS, CD; ANTIGENS, CD13; ANTIGENS, THY-1; CARCINOMA, HEPATOCELLULAR; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL SEPARATION; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; HUMANS; LIVER NEOPLASMS; NEOPLASTIC STEM CELLS; PEPTIDES;

EID: 84898906313     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/jgh.12484     Document Type: Article

References (37)

1. Clarke MF, Dick JE, Dirks PB etal. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006; 66: 9339-9344.
2. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N. Engl. J. Med. 2006; 355: 1253-1261.
3. Marquardt JU, Factor VM, Thorgeirsson SS. Epigenetic regulation of cancer stem cells in liver cancer: current concepts and clinical implications. J. Hepatol. 2010; 53: 568-577.
4. Lapidot T, Sirard C, Vormoor J etal. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367: 645-648.
5. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997; 3: 730-737.
6. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005; 65: 10946-10951.
7. Houghton J, Stoicov C, Nomura S etal. Gastric cancer originating from bone marrow-derived cells. Science 2004; 306: 1568-1571.
8. Kim CF, Jackson EL, Woolfenden AE etal. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005; 121: 823-835.
9. Ponti D, Costa A, Zaffaroni N etal. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005; 65: 5506-5511.
10. Ricci-Vitiani L, Lombardi DG, Pilozzi E etal. Identification and expansion of human colon-cancer-initiating cells. Nature 2007; 445: 111-115.
11. Singh SK, Clarke ID, Terasaki M etal. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003; 63: 5821-5828.
12. Falciatori I, Borsellino G, Haliassos N etal. Identification and enrichment of spermatogonial stem cells displaying side-population phenotype in immature mouse testis. FASEB J. 2004; 18: 376-378.
13. 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.
14. Shimano K, Satake M, Okaya A etal. Hepatic oval cells have the side population phenotype defined by expression of ATP-binding cassette transporter ABCG2/BCRP1. Am. J. Pathol. 2003; 163: 3-9.
15. Kondo T, Setoguchi T, Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc. Natl Acad. Sci. U.S.A. 2004; 101: 781-786.
16. Chiba T, Kita K, Zheng YW etal. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology 2006; 44: 240-251.
17. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res. 2005; 65: 6207-6219.
18. Itsubo M, Ishikawa T, Toda G, Tanaka M. Immunohistochemical study of expression and cellular localization of the multidrug resistance gene product P-glycoprotein in primary liver carcinoma. Cancer 1994; 73: 298-303.
19. Park CY, Tseng D, Weissman IL. Cancer stem cell-directed therapies: recent data from the laboratory and clinic. Mol. Ther. 2009; 17: 219-230.
20. Haraguchi N, Ishii H, Mimori K etal. CD13 is a therapeutic target in human liver cancer stem cells. J. Clin. Invest. 2010; 120: 3326-3339.
21. Ma S, Chan KW, Hu L etal. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007; 132: 2542-2556.
22. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem. Biophys. Res. Commun. 2006; 351: 820-824.
23. Yamashita T, Ji J, Budhu A etal. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 2009; 136: 1012-1024.
24. Yang ZF, Ho DW, Ng MN etal. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 2008; 13: 153-166.
25. Libbrecht L. Hepatic progenitor cells in human liver tumor development. World J. Gastroenterol. 2006; 12: 6261-6265.
26. Yano H, Iemura A, Fukuda K, Mizoguchi A, Haramaki M, Kojiro M. Establishment of two distinct human hepatocellular carcinoma cell lines from a single nodule showing clonal dedifferentiation of cancer cells. Hepatology 1993; 18: 320-327.
27. Hisaka T, Yano H, Ogasawara S etal. Interferon-alphaCon1 suppresses proliferation of liver cancer cell lines in vitro and in vivo. J. Hepatol. 2004; 41: 782-789.
28. Yano H, Iemura A, Haramaki M etal. Interferon alfa receptor expression and growth inhibition by interferon alfa in human liver cancer cell lines. Hepatology 1999; 29: 1708-1717.
29. Ueda K, Ogasawara S, Akiba J etal. Aldehyde dehydrogenase 1 identifies cells with cancer stem cell-like properties in a human renal cell carcinoma cell line. PLOS ONE 2013; 8: e75463.
30. Burkert J, Otto WR, Wright NA. Side populations of gastrointestinal cancers are not enriched in stem cells. J. Pathol. 2008; 214: 564-573.
31. Sell S, Leffert HL. Liver cancer stem cells. J. Clin. Oncol. 2008; 26: 2800-2805.
32. Breuhahn K, Longerich T, Schirmacher P. Dysregulation of growth factor signaling in human hepatocellular carcinoma. Oncogene 2006; 25: 3787-3800.
33. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007; 132: 2557-2576.
34. Tannapfel A, Busse C, Weinans L etal. INK4a-ARF alterations and p53 mutations in hepatocellular carcinomas. Oncogene 2001; 20: 7104-7109.
35. Teufel A, Staib F, Kanzler S, Weinmann A, Schulze-Bergkamen H, Galle PR. Genetics of hepatocellular carcinoma. World J. Gastroenterol. 2007; 13: 2271-2282.
36. van Zijl F, Zulehner G, Petz M etal. Epithelial-mesenchymal transition in hepatocellular carcinoma. Future Oncol. 2009; 5: 1169-1179.
37. Villanueva A, Newell P, Chiang DY, Friedman SL, Llovet JM. Genomics and signaling pathways in hepatocellular carcinoma. Semin. Liver Dis. 2007; 27: 55-76.