Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines

Lu Cao1, Yanming Zhou2, Beibei Zhai1, Jian Liao1, Wen Xu1, Ruixiu Zhang1, Jing Li1, Yu Zhang1, Lei Chen1, Haihua Qian1, Mengchao Wu1, Zheng Yin1
1Department of Molecular Oncology, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China
2Department of Hepato-Biliary-Pancreato-Vascular Surgery, the First affiliated Hospital of Xiamen University, Xiamen, China

Tóm tắt

Abstract Background

Cancer stem cells (CSCs) are regarded as the cause of tumor formation and recurrence. The isolation and identification of CSCs could help to develop novel therapeutic strategies specifically targeting CSCs.

Methods

Human hepatoma cell lines were plated in stem cell conditioned culture system allowed for sphere forming. To evaluate the stemness characteristics of spheres, the self-renewal, proliferation, chemoresistance, tumorigenicity of the PLC/PRF/5 sphere-forming cells, and the expression levels of stem cell related proteins in the PLC/PRF/5 sphere-forming cells were assessed, comparing with the parental cells. The stem cell RT-PCR array was performed to further explore the biological properties of liver CSCs.

Results

The PLC/PRF/5, MHCC97H and HepG2 cells could form clonal nonadherent 3-D spheres and be serially passaged. The PLC/PRF/5 sphere-forming cells possessed a key criteria that define CSCs: persistent self-renewal, extensive proliferation, drug resistance, overexpression of liver CSCs related proteins (Oct3/4, OV6, EpCAM, CD133 and CD44). Even 500 sphere-forming cells were able to form tumors in NOD/SCID mice, and the tumor initiating capability was not decreased when spheres were passaged. Besides, downstream proteins DTX1 and Ep300 of the CSL (CBF1 in humans, Suppressor of hairless in Drosophila and LAG1 in C. elegans) -independent Notch signaling pathway were highly expressed in the spheres, and a gamma-secretase inhibitor MRK003 could significantly inhibit the sphere formation ability.

Conclusions

Nonadherent tumor spheres from hepatoma cell lines cultured in stem cell conditioned medium possess liver CSC properties, and the CSL-independent Notch signaling pathway may play a role in liver CSCs.

Từ khóa


Tài liệu tham khảo

Parkin DM: Global cancer statistics in the year 2000. Lancet Oncol. 2001, 2: 533-543. 10.1016/S1470-2045(01)00486-7.

El-Serag HB, Rudolph KL: Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007, 132: 2557-2576. 10.1053/j.gastro.2007.04.061.

Altekruse SF, McGlynn KA, Reichman ME: Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005. J Clin Oncol. 2009, 27: 1485-1491. 10.1200/JCO.2008.20.7753.

Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Chu PW, Lam CT, Poon RT, Fan ST: Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell. 2008, 13: 153-166. 10.1016/j.ccr.2008.01.013.

Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, Zheng BJ, Guan XY: Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology. 2007, 132: 2542-2556. 10.1053/j.gastro.2007.04.025.

Zhu Z, Hao X, Yan M, Yao M, Ge C, Gu J, Li J: Cancer stem/progenitor cells are highly enriched in CD133+CD44+ population in hepatocellular carcinoma. Int J Cancer. 2010, 126: 2067-2078.

Kimura O, Takahashi T, Ishii N, Inoue Y, Ueno Y, Kogure T, Fukushima K, Shiina M, Yamagiwa Y, Kondo Y, Inoue J, Kakazu E, Iwasaki T, Kawagishi N, Shimosegawa T, Sugamura K: Characterization of the epithelial cell adhesion molecule (EpCAM)+ cell population in hepatocellular carcinoma cell lines. Cancer Sci. 2010, 101: 2145-2155. 10.1111/j.1349-7006.2010.01661.x.

Yang W, Yan HX, Chen L, Liu Q, He YQ, Yu LX, Zhang SH, Huang DD, Tang L, Kong XN, Chen C, Liu SQ, Wu MC, Wang HY: Wnt/beta-catenin signaling contributes to activation of normal and tumorigenic liver progenitor cells. Cancer Res. 2008, 68: 4287-4295. 10.1158/0008-5472.CAN-07-6691.

Haraguchi N, Ishii H, Mimori K, Tanaka F, Ohkuma M, Kim HM, Akita H, akiuchi D, Hatano H, Nagano H, Barnard GF, Doki Y, Mori M: CD13 is a therapeutic target in human liver cancer stem cells. J Clin Invest. 2010, 120: 3326-3339. 10.1172/JCI42550.

Sell S, Leffert HL: Liver cancer stem cells. J Clin Oncol. 2008, 26: 2800-2805. 10.1200/JCO.2007.15.5945.

Wu Y, Wu PY: CD133 as a marker for cancer stem cells: progresses and concerns. Stem Cells Dev. 2009, 18: 1127-1134. 10.1089/scd.2008.0338.

Salnikov AV, Kusumawidjaja G, Rausch V, Bruns H, Gross W, Khamidjanov A, Ryschich E, Gebhard MM, Moldenhauer G, Büchler MW, Schemmer P, Herr I: Cancer stem cell marker expression in hepatocellular carcinoma and liver metastases is not sufficient as single prognostic parameter. Cancer Lett. 2009, 275: 185-193. 10.1016/j.canlet.2008.10.015.

Reynolds BA, Weiss S: Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol. 1996, 175: 1-13. 10.1006/dbio.1996.0090.

Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha M: In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003, 17: 1253-1270. 10.1101/gad.1061803.

Suzuki A, Oyama K, Fukao K, Nakauchi H, Taniguchi H: Establishment of clonal colony-forming assay system for pancreatic stem/progenitor cells. Cell Transplant. 2002, 11: 451-453.

Bez A, Corsini E, Curti D, Biggiogera M, Colombo A, Nicosia RF, Pagano SF, Parati EA: Neurosphere and neurosphere-forming cells: morphological and ultrastructural characterization. Brain Res. 2003, 993: 18-29. 10.1016/j.brainres.2003.08.061.

Shi X, Gipp J, Bushman W: Anchorage-independent culture maintains prostate stem cells. Dev Biol. 2007, 312: 396-406. 10.1016/j.ydbio.2007.09.042.

Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks P: Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003, 63: 5821-5828.

Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone M: Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005, 65: 5506-5511. 10.1158/0008-5472.CAN-05-0626.

Gibbs CP, Kukekov VG, Reith JD, Tchigrinova O, Suslov ON, Scott EW, Ghivizzani SC, Ignatova TN, Steindler DA: Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia. 2005, 7: 967-976. 10.1593/neo.05394.

Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz S, Van Belle PA, Xu X, Elder DE, Herlyn M: A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 2005, 65: 9328-9337. 10.1158/0008-5472.CAN-05-1343.

Gou S, Liu T, Wang C, Yin T, Li K, Yang M, Zhou J: Establishment of clonal colony-forming assay for propagation of pancreatic cancer cells with stem cell properties. Pancreas. 2007, 34: 429-435. 10.1097/MPA.0b013e318033f9f4.

Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, Nephew KP: Identification and Characterization of Ovarian Cancer-Initiating Cells from Primary Human Tumors. Cancer Res. 2008, 68: 4311-4320. 10.1158/0008-5472.CAN-08-0364.

Fujii H, Honoki K, Tsujiuchi T, Kido A, Yoshitani K, Takakura Y: Sphere-forming stem-like cell populations with drug resistance in human sarcoma cell lines. Int J Oncol. 2009, 34: 1381-1386.

Rappa G, Mercapide J, Anzanello F, Prasmickaite L, Xi Y, Ju J, Fodstad O, Lorico A: Growth of cancer cell lines under stem cell-like conditions has the potential to unveil therapeutic targets. Exp Cell Res. 2008, 314: 2110-2122. 10.1016/j.yexcr.2008.03.008.

Dunsford HA, Sell S: Production of monoclonal antibodies to preneoplastic liver cell populations induced by chemical carcinogens in rats and to transplantable Morris hepatomas. Cancer Res. 1989, 49: 4887-4893.

Strain AJ, Crosby HA, Nijjar S, Kelly DA, Hubscher SG: Human liver-derived stem cells. Semin Liver Dis. 2003, 23: 373-384.

Van Den Heuvel MC, Slooff MJ, Visser L, Muller M, De Jong KP, Poppema S, Gouw AS: Expression of anti-OV6 antibody and anti-N-CAM antibody along the biliary line of normal and diseased human livers. Hepatology. 2001, 33: 1387-1393. 10.1053/jhep.2001.24453.

Michelson S, Slate D: Emergence of the drug-resistant phenotype in tumor subpopulations: a hybrid model. J Natl Cancer Inst. 1989, 81: 1392-1401. 10.1093/jnci/81.18.1392.

Perryman SV, Sylvester KG: Repair and regeneration: opportunities for carcinogenesis from tissue stem cells. J Cell Mol Med. 2006, 10: 292-308. 10.1111/j.1582-4934.2006.tb00400.x.

Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, Iwama A, Nakauchi H, Taniguchi H: Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology. 2006, 44: 240-251.

Shen G, Shen F, Shi Z, Liu W, Hu W, Zheng X, Wen L, Yang X: Identification of cancer stem-like cells in the C6 glioma cell line and the limitation of current identification methods. Vitro Cell Dev Biol Anim. 2008, 44: 280-289. 10.1007/s11626-008-9115-z.

Pardal R, Clarke MF, Morrison SJ: Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 2003, 3: 895-902. 10.1038/nrc1232.

Marx J: Cancer research. Mutant stem cells may seed cancer. Science. 2003, 301: 1308-1310. 10.1126/science.301.5638.1308.

Hansford LM, McKee AE, Zhang L, George RE, Gerstle JT, Thorner PS, Smith KM, Look AT, Yeger H, Miller FD, Irwin MS, Thiele CJ, Kaplan DR: Neuroblastoma cells isolated from bone marrow metastases contain a naturally enriched tumor-initiating cell. Cancer Res. 2007, 67: 11234-11243. 10.1158/0008-5472.CAN-07-0718.

Duncan AW, Rattis FM, DiMascio LN, Congdon KL, Pazianos G, Zhao C, Yoon K, Cook JM, Willert K, Gaiano N, Reya T: Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol. 2005, 6: 314-322. 10.1038/ni1164.

Stier S, Cheng T, Dombkowski D, Carlesso N, Scadden DT: Notch1 activation increases hematopoietic stem cell self-renewal in vivo and favors lymphoid over myeloid lineage outcome. Blood. 2002, 99: 2369-2378. 10.1182/blood.V99.7.2369.

Pinnix CC, Herlyn M: The many faces of Notch signaling in skin-derived cells. Pigment Cell Res. 2007, 20: 458-465. 10.1111/j.1600-0749.2007.00410.x.

van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, Clevers H: Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature. 2005, 435: 959-963. 10.1038/nature03659.

Martinez Arias A, Zecchini V, Brennan K: CSL-independent Notch signaling: a checkpoint in cell fate decisions during development?. Curr Opin Genet Dev. 2002, 12: 524-533. 10.1016/S0959-437X(02)00336-2.

Yamamoto N, Yamamoto S, Inagaki F: Role of Deltex-1 as a transcriptional regulator downstream of the Notch receptor. J Biol Chem. 2001, 276: 45031-45040. 10.1074/jbc.M105245200.