CD34+ Liver Cancer Stem Cells Were Formed by Fusion of Hepatobiliary Stem/Progenitor Cells with Hematopoietic Precursor-Derived Myeloid Intermediates

Stem Cells and Development

Volumn 24, Issue 21, 2015, Pages 2467-2478

  Zeng, Changjun ^a,b   Zhang, Yanling ^a,c   Park, Su Cheol ^a,d   Eun, Jong Ryeol ^a,e   Nguyen, Ngoc Tue ^a   Tschudy Seney, Benjamin ^a   Jung, Yong Jin ^a,f   Theise, Neil D ^g   Zern, Mark A ^a   Duan, Yuyou ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SICHUAN AGRICULTURAL UNIVERSITY   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

^d Korea Institute of Radiation and Medical Science   (South Korea)

^e Yeungnam University College of Medicine   (South Korea)

^f Seoul National University   (South Korea)

^g ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ALPHA 1 ANTITRYPSIN; ALPHA FETOPROTEIN; ANTIGEN; CD14 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; CD68 ANTIGEN; CISPLATIN; GAMMA INTERFERON; INTERLEUKIN 12P35; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; LYSOZYME; MACROPHAGE ANTIGEN; MONOCYTE CHEMOTACTIC PROTEIN 1; OV6 PROTEIN; PROTEIN; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS DNA; CYTOKINE; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ARTICLE; CANCER RESISTANCE; CANCER STEM CELL; CELL FUNCTION; CELL FUSION; CELL ISOLATION; CELL LINEAGE; CHROMOSOME; CHROMOSOME ANALYSIS; CONTROLLED STUDY; DNA INTEGRATION; ESCHERICHIA COLI; HEMATOPOIETIC STEM CELL; HEPATITIS B VIRUS; HEPATOBILIARY STEM PROGENITOR CELL; HUMAN; HUMAN CELL; LIVER CANCER; LIVER CANCER STEM CELL; MOUSE; MUTATION; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; XENOGRAFT; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; IMMUNOLOGY; LIVER; LIVER TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; STEM CELL;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD34; CELL DIFFERENTIATION; CYTOKINES; HEMATOPOIETIC STEM CELLS; HUMANS; INTERLEUKIN-6; LIVER; LIVER NEOPLASMS; MICE; NEOPLASTIC STEM CELLS; STEM CELLS;

EID: 84945418363     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2015.0202     Document Type: Article

References (51)

1. Reya T, SJ Morrison, MF Clark and IL Weissman. (2001). Stem cell, cancer and cancer stem cells. Nature 414:105-111.
2. Driessens G, B Beck, A Caauwe, BD Simons and C Blanpain. (2012). Defining the mode of tumor growth by clonal analysis. Nature 488:527-530.
3. Schepers AG, HJ Snippert, DE Stange, M van den Born, JH van Es, M van de Wetering and H Clevers. (2012). Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 337:730-735.
4. Chen J, Y Li, T Yu, MR McKay, KD Burns, SG Kernie and LF Parada. (2012). A restricted cell population propagate glioblastoma growth after chemotherapy. Nature 488:522-526.
5. Chiba T, YW Zheng, K Kita, O Yokosuka, H Saisho, M Onodera, H Miyoshi, M Nakano, Y Zen, et al. (2007). Enhanced self-renewal capability in hepatic stem/progenitor cells drives cancer initiation. Gastroenterology 133:937-950.
6. Guo W, JL Lasky, C Chang, S Mosessian, X Lewis, Y Xiao, JE Yeh, JY Chen, ML Iruela-Arispe, M Varella-Garcia and H Wu. (2008). Multi-genetic events collaboratively contribute to Pten-null leukaemia stem-cell formation. Nature 453:529-533.
7. Friedman-Morvinski D and IM Verma. (2014). Dedifferentiation and reprogramming: origins of cancer stem cells. EMBO Rep 15:244-253.
8. Yao Z and L Mishra. (2009). Cancer stem cells and hepatocellular carcinoma. Cancer Biol Ther 8:1691-1698.
9. Wu X and D Chen. (2006). Origin of hepatocellular carcinoma: role of stem cells. J Gastroenterol Hepatol 21:1093-1098.
10. Cogle CR, ND Theise, D Fu, D Ucar, S Lee, SM Guthrie, J Lonergan, W Rybka, DS Krause and EW Scott. (2007). Bone marrow contributes to epithelial cancers in mice and humans as developmental mimicry. Stem Cells 25:1881-1887.
11. Houghton J, C Stoicov, S Nomura, AB Rogers, J Carlson, H Li, X Cai, JG Fox, JR Goldenring and TC Wang. (2004). Gastric cancer originating from bone marrow-derived cells. Science 306:1568-1571.
12. Yang ZF, DW Ho, MN Ng, CK Lau, WC Yu, P Ngai, PW Chu, CT Lam, RT Poon and ST Fan. (2008). Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13:153-166.
13. Zhu Z, X Hao, M Yan, M Yao, C Ge, J Gu and J Li. (2009). Cancer stem/progenitor cells are highly enriched in CD133(+) CD44(+) population in hepatocellular carcinoma. Int J Cancer 126:2067-2078.
14. Yamashita T, J Ji, A Budhu, M Forgues, W Yang, HY Wang, H Jia, Q Ye, LX Qin, et al. (2009). EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 136: 1012-1024.
15. Duncan AW, C Dorrell and M Grompe. (2009). Stem cells and liver regeneration. Gastroenterology 137:466-481.
16. Eckersley-Maslin MA, FJ Warner, CA Grzelak, GW McCaughan and NA Shackel. (2009). Bone marrow stem cells and the liver: Are they relevant J Gastroenterol Hepatol 24:1608-1616.
17. Park SC, NT Nguyen, JR Eun, Y Zhang, YJ Jung, B Tschudy-Seney, A Trotsyuk, A Lam, R Ramsamooj, et al. (2015). Identification of cancer stem cell subpopulations of CD34+ PLC/PRF/5 that result in three types of human liver carcinomas. Stem Cells Dev 24:1008-1021.
18. Park SC, C Zeng, B Tschudy-Seney, NT Nguyen, JR Eun, Y Zhang, R Ramsamooj, Y Zhang, M Zhao, et al. (2015). Clonogenically culturing and expanding CD34+ liver cancer stem cells in vitro. Stem Cells Dev 24:1506-1514.
19. Duan Y, X Ma, W Zou, C Wang, IS Bahbahan, TP Ahuja, V Tolstikov and MA Zern. (2010). Differentiation and characterization of metabolically functioning hepatocytes from human embryonic stem cells. Stem Cells 28:674-686.
20. Lo Y, WZ Mehal and KA Fleming. (1989). In vitro amplification of hepatitis B virus sequences from liver tumor DNA and from paraffin wax embedded tissue using the polymerase chain reaction. J Clin Pathol 42:840-846.
21. Koch S, AF von Loringhoven, PH Hofschneider and R Koshy. (1984). Amplification and rearrangement in hepatoma cell DNA associated with integrated hepatitis B virus DNA. EMBO J 3:2185-2189.
22. Rivkina MB, VG Lunin, AM Mahov, TI Tikchonenko and RA Kukain. (1988). Nucleotide sequence of integrated hepatitis B virus DNA and human flanking regions in the genome of the PLC/PRF/5 cell line. Gene 64:285-296.
23. Seabright M. (1971). A rapid banding technique for human chromosomes. Lancet 2:971-972.
24. Sell S and HA Dunsford. (1989). Evidence for the stem cell origin of hepatocellular carcinoma and cholangiocarcinoma. Am J Pathol 134:1347-1363.
25. Theise ND, R Saxena, BC Portmann, SN Thung H Yee, L Chiriboga, A Kumar and JM Crawford. (1999). The canals of Hering and hepatic stem cells in human. Hepatology 30:1425-1433.
26. Arii S and M Imamura. (2007). Physiological role of sinusoidal endothelial cells and Kupffer cells and their implication in the pathogenesis of liver injury. J Hepatobiliary Pancreat Surg 7:40-48.
27. Pinto MR, E Bey and R Bernstein. (1985). The PLC/PRF/5 human hepatoma cell line. I. Reevaluation of the karyotype. Cancer Genet Cytogenet 18:11-18.
28. Willenbring H, AS Bailey, M Foster, Y Akkari, C Dorrell, S Olson, M Finegold, WH Fleming and M Grompe. (2004). Myelomonocytic cells are sufficient for therapeutic cell fusion in the liver. Nat Med 10:744-748.
29. Wang X, H Willenbring, Y Akkari, Y Torimaru, M Foster, M Al-Dhalimy, E Lagasse, M Finegold, S Olson and M Grompe. (2003). Cell fusion is the principal source of bonemarrow-derived hepatocytes. Nature 422:897-901.
30. Handgretinger R and S Kuçi. (2013). CD133-positive hematopoietic stem cells: from biology to medicine. Adv Exp Med Biol 777:99-111.
31. Carpino G, V Cardinale, L Reid, D Alvaro and E Gaudio. (2012). Cell of origin and cancer stem cells in cholangiocarcinoma. Transl Gastrointest Cancer 1:33-43.
32. Knowles BB, CC Howe and DP Aden. (1980). Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science 209:497-499.
33. Jang Y, MI Collector, SB Baylin, AM Diehl and SJ Sharkis. (2004). Hematopoietic stem cells convert into liver cells within days without fusion. Nat Cell Biol 6:532-539.
34. Lagasse E, H Connors, M Al-Dhalimy, M Reitsma, M Dohse, L Osborne, X Wang, M Finegold, IL Weissman and M Grompe. (2000). Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 6:229-1234.
35. Theise ND, M Nimmakayalu, R Gardner, PB Illei, G Morgan, L Teperman,OHenegariu and DS Krause. (2003). Liver from bone marrow in humans. Hepatology 32:11-16.
36. Fogt F, KH Beyser, C Poremba, RL Zimmerman, U Khettry and J Ruschoff. (2000). Recipient-derived hepatocytes in liver transplants: a rare event in sex-mismatched transplants. Hepatology 36:173-176.
37. Kö rbling M, RL Katz, A Khanna, AC Ruifrok, G Rondon, M Albitar, RE Champlin and Z Estrov. (2002). Hepatocytes and epithelial cells of donor origin in recipients of peripheral blood stem cells. N Engl J Med 346: 738-746.
38. Idilman R, E Erden, I Kuzu, S Ersoz, Z Karasu, K Karayalcin, G Yuce, Y Tokat, Y Sahin, et al. (2004). Recipientderived hepatocytes in sex-mismatched liver allografts after liver transplantation: early versus late transplant biopsies. Transplantation 78:1647-1652.
39. Petersen BE, WC Bowen, KD Patrene, WM Mars, AK Sullivan, N Murase, SS Boggs, JS Greenberger and JP Goff. (1999). Bone marrow as a potential source of hepatic oval cells. Science 284:1168-1170.
40. Alexander JJ, EM Bey, EW Geddes and G Lecatsas. (1976). Establishment of a continuously growing cell line from primary carcinoma of the liver. S Afr Med J 50:2124-2128.
41. Kollet O, S Shivtiel, YQ Chen, J Suriawinata, SN Thung, MD Dabeva, J Kahn, A Spiegel, A Dar, et al. (2003). HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34+ stem cell recruitment to the liver. J Clin Invest 112:160-169.
42. Lazova R, GS Laberge, E Duvall, N Spoelstra, V Klump, M Sznol, D Cooper, RA Spritz, JT Chang and JM Pawelek. (2013). A melanoma brain metastasis with a donor-patient hybrid genome following bone marrow transplantation: first evidence for fusion in human cancer. PLoS One 8:e66731.
43. Pawelek JM and AK Chakraborty. (2008). Fusion of tumor cells with bone marrow-derived cells: a unifying explanation for metastasis. Nat Rev Cancer 8:377-386.
44. Ding J, W Jin, C Chen, Z Shao and J Wu. (2012). Tumor associated macrophage x cancer cell hybrids may acquire cancer stem cell properties in breast cancer. PLoS One 7:e41942.
45. Bjerkvig R, BB Tysnes, KS Aboody, J Najbauer and AJ Terzis. (2005). The origin of the cancer stem cell: current controversies and new insights. Nat Rev Cancer 5:899-904.
46. Alvarez-Dolado M, R Pardal, JM Garcia-Verdugo, JR Fike, HO Lee, K Pfeffer, C Lois, SJ Morrison and A Alvarez-Buylla. (2003). Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425:968-973.
47. Zhang S, D Wang, Z Estrov, S Raj, JT Willerson and ET Yeh. (2004). Both cell fusion and transdifferentiation account for the transformation of human peripheral blood CD34-positive cells into cardiomyocytes in vivo. Circulation 110:3803-3807.
48. Lluis F and MP Cosma. (2011). Cell-fusion-mediated somatic-cell reprogramming: a mechanism for tissue regeneration. J Cell Physiol 223:6-13.
49. Itakura E, RR Huang, DR Wen and AJ Cochran. (2011). "Stealth" melanoma cells in histology-negative sentinel lymph nodes. Am J Surg Pathol 35:1657-1665.
50. Chakraborty A, R Lazova, S Davies, H Bäckvall, F Ponten, D Brash and J Pawelek. (2004). Donor DNA in a renal cell carcinoma metastasis from a bone marrow transplant recipient. Bone Marrow Transplant 34:183-186.
51. Clawson GA, E Kimchi, SD Patrick, P Xin, R Harouaka, S Zheng, A Berg, T Schell, KF Staveley-O'Carroll, et al. (2012). Circulating tumor cells in melanoma patients. PLoS One 7:e41052.