Arsenic trioxide induces differentiation of CD133+ hepatocellular carcinoma cells and prolongs posthepatectomy survival by targeting GLI1 expression in a mouse model

Journal of Hematology and Oncology

Volumn 7, Issue 1, 2014, Pages

  Zhang, Ke Zhi ^a   Zhang, Qiang Bo ^a,b   Zhang, Quan Bao ^a   Sun, Hui Chuan ^a   Ao, Jian Yang ^a   Chai, Zong Tao ^a   Zhu, Xiao Dong ^a   Lu, Lu ^a   Zhang, Yuan Yuan ^a   Bu, Yang ^a   Kong, Ling Qun ^a   Tang, Zhao You ^a  

^a FUDAN UNIVERSITY   (China)

^b SHANDONG UNIVERSITY   (China)

Author keywords

Arsenic trioxide; Cancer stem cell; Differentiation; GLI1; Hepatocellular carcinoma

Indexed keywords

ARSENIC TRIOXIDE; CD133 ANTIGEN; TRANSCRIPTION FACTOR GLI1; GLI1 PROTEIN, HUMAN; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; ORGANOARSENIC DERIVATIVE; OXIDE; PEPTIDE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CANCER SURGERY; CARCINOGENICITY; CARCINOMA CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; LIVER RESECTION; MALE; MOUSE; MOUSE MODEL; NONHUMAN; POSTOPERATIVE PERIOD; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SURVIVAL RATE; TUMOR RECURRENCE; TUMOR XENOGRAFT; ANIMAL; BIOSYNTHESIS; CARCINOMA, HEPATOCELLULAR; DISEASE MODEL; DOWN REGULATION; DRUG EFFECTS; DRUG SCREENING; GENETICS; LIVER NEOPLASMS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; RANDOMIZATION; SCID MOUSE; SIGNAL TRANSDUCTION; SURVIVAL; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD; ARSENICALS; CARCINOMA, HEPATOCELLULAR; CELL DIFFERENTIATION; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GLYCOPROTEINS; HUMANS; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM RECURRENCE, LOCAL; NEOPLASTIC STEM CELLS; OXIDES; PEPTIDES; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TRANSCRIPTION FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84899126505     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/1756-8722-7-28     Document Type: Article

References (47)

1. Global cancer statistics. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D, CA Cancer J Clin 2011 61 69 90 10.3322/caac.20107 21296855
2. Continuous improvement of survival outcomes of resection of hepatocellular carcinoma: a 20-year experience. Fan ST, Mau Lo C, Poon RT, Yeung C, Leung Liu C, Yuen WK, Ming Lam C, Ng KK, Ching Chan S, Ann Surg 2011 253 745 758 10.1097/SLA.0b013e3182111195 21475015
3. Prediction of posthepatectomy recurrence of hepatocellular carcinoma by circulating cancer stem cells: a prospective study. Fan ST, Yang ZF, Ho DW, Ng MN, Yu WC, Wong J, Ann Surg 2011 254 569 576 10.1097/SLA.0b013e3182300a1d 21892074
4. Silencing or fueling metastasis with VEGF inhibitors: antiangiogenesis revisited. Loges S, Mazzone M, Hohensinner P, Carmeliet P, Cancer cell 2009 15 167 170 10.1016/j.ccr.2009.02.007 19249675
5. Sorafenib down-regulates expression of HTATIP2 to promote invasiveness and metastasis of orthotopic hepatocellular carcinoma tumors in mice. Zhang W, Sun HC, Wang WQ, Zhang QB, Zhuang PY, Xiong YQ, Zhu XD, Xu HX, Kong LQ, Wu WZ, Wang L, Song TQ, Li Q, Tang ZY, Gastroenterology 2012 143 1641 1649 e1645 10.1053/j.gastro.2012.08.032 22922424
6. Molecular targeted therapy for hepatocellular carcinoma in the current and potential next strategies. Tanaka S, Arii S, J Gastroenterol 2011 46 289 296 10.1007/s00535-011-0387-9 21350811
7. Cancer stem cells. Jordan CT, Guzman ML, Noble M, N Engl J Med 2006 355 1253 1261 10.1056/NEJMra061808 16990388
8. Biology of hepatic cancer stem cells. Tong CM, Ma S, Guan XY, J Gastroenterol Hepatol 2011 26 1229 1237 10.1111/j.1440-1746.2011.06762.x 21557770
9. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H, Biochem Biophys Res Commun 2006 351 820 824 10.1016/j.bbrc.2006.10. 128 17097610
10. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Yin S, Li J, Hu C, Chen X, Yao M, Yan M, Jiang G, Ge C, Xie H, Wan D, Yang S, Zheng S, Gu J, Int J Cancer J int du cancer 2007 120 1444 1450 10.1002/ijc.22476
11. CD133(+) liver tumor-initiating cells promote tumor angiogenesis, growth, and self-renewal through neurotensin/interleukin-8/CXCL1 signaling. Tang KH, Ma S, Lee TK, Chan YP, Kwan PS, Tong CM, Ng IO, Man K, To KF, Lai PB, Lo CM, Guan XY, Chan KW, Hepatology 2012 55 807 820 10.1002/hep.24739 21994122
12. CD133+ liver cancer stem cells modulate radioresistance in human hepatocellular carcinoma. Piao LS, Hur W, Kim TK, Hong SW, Kim SW, Choi JE, Sung PS, Song MJ, Lee BC, Hwang D, Yoon SK, Cancer Lett 2012 315 129 137 10.1016/j.canlet.2011.10.012 22079466
13. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, Zheng BJ, Guan XY, Gastroenterology 2007 132 2542 2556 10.1053/j.gastro.2007.04.025 17570225
14. Differentiation therapy of acute promyelocytic leukemia with tretinoin (all-trans-retinoic acid). Warrell RP Jr, Frankel SR, Miller WH Jr, Scheinberg DA, Itri LM, Hittelman WN, Vyas R, Andreeff M, Tafuri A, Jakubowski A, Gabrilove J, Gordon MS, Dmitrovsky E, N Engl J Med 1991 324 1385 1393 10.1056/NEJM199105163242002 1850498
15. Hedgehog signaling in development and cancer. Jiang J, Hui CC, Dev Cell 2008 15 801 812 10.1016/j.devcel.2008.11.010 19081070
16. Expression and clinical significance of the stem cell marker CD133 in hepatocellular carcinoma. Song W, Li H, Tao K, Li R, Song Z, Zhao Q, Zhang F, Dou K, Int J Clin Pract 2008 62 1212 1218 10.1111/j.1742-1241.2008.01777.x 18479363
17. Cancer stem cell gene profile as predictor of relapse in high risk stage II and stage III, radically resected colon cancer patients. Giampieri R, Scartozzi M, Loretelli C, Piva F, Mandolesi A, Lezoche G, Del Prete M, Bittoni A, Faloppi L, Bianconi M, Cecchini L, Guerrieri M, Bearzi I, Cascinu S, PloS one 2013 8 72843 10.1371/journal.pone.0072843 24023782
18. Differentiation therapy of hepatocellular carcinoma in mice with recombinant adenovirus carrying hepatocyte nuclear factor-4alpha gene. Yin C, Lin Y, Zhang X, Chen YX, Zeng X, Yue HY, Hou JL, Deng X, Zhang JP, Han ZG, Xie WF, Hepatology 2008 48 1528 1539 10.1002/hep.22510 18925631
19. BMP4 administration induces differentiation of CD133+ hepatic cancer stem cells, blocking their contributions to hepatocellular carcinoma. Zhang L, Sun H, Zhao F, Lu P, Ge C, Li H, Hou H, Yan M, Chen T, Jiang G, Xie H, Cui Y, Huang X, Fan J, Yao M, Li J, Cancer Res 2012 72 4276 4285 10.1158/0008-5472.CAN-12- 1013 22773665
20. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. Varnat F, Duquet A, Malerba M, Zbinden M, Mas C, Gervaz P, Ruiz I, Altaba A, EMBO Mol Med 2009 1 338 351 10.1002/emmm.200900039 20049737
21. Sonic hedgehog pathway is essential for maintenance of cancer stem-like cells in human gastric cancer. Song Z, Yue W, Wei B, Wang N, Li T, Guan L, Shi S, Zeng Q, Pei X, Chen L, PloS one 2011 6 17687 10.1371/journal.pone.0017687 21394208
22. Inhibition of CK2alpha down-regulates Hedgehog/Gli signaling leading to a reduction of a stem-like side population in human lung cancer cells. Zhang S, Wang Y, Mao JH, Hsieh D, Kim IJ, Hu LM, Xu Z, Long H, Jablons DM, You L, PloS one 2012 7 38996 10.1371/journal.pone.0038996 22768056
23. GANT-61 inhibits pancreatic cancer stem cell growth in vitro and in NOD/SCID/IL2R gamma null mice xenograft. Fu J, Rodova M, Roy SK, Sharma J, Singh KP, Srivastava RK, Shankar S, Cancer Lett 2013 330 22 32 10.1016/j.canlet.2012. 11.018 23200667
24. Hedgehog-GLI signaling drives self-renewal and tumorigenicity of human melanoma-initiating cells. Santini R, Vinci MC, Pandolfi S, Penachioni JY, Montagnani V, Olivito B, Gattai R, Pimpinelli N, Gerlini G, Borgognoni L, Stecca B, Stem Cells 1808-1818 2012 30
25. Inhibition of the hedgehog pathway in advanced basal-cell carcinoma. Von Hoff DD, LoRusso PM, Rudin CM, Reddy JC, Yauch RL, Tibes R, Weiss GJ, Borad MJ, Hann CL, Brahmer JR, Mackey HM, Lum BL, Darbonne WC, Marsters JC Jr, de Sauvage FJ, Low JA, N Engl J Med 2009 361 1164 1172 10.1056/NEJMoa0905360 19726763
26. High expression of patched homolog-1 messenger RNA and glioma-associated oncogene-1 messenger RNA of sonic hedgehog signaling pathway indicates a risk of postresection recurrence of hepatocellular carcinoma. Jeng KS, Sheen IS, Jeng WJ, Lin CC, Lin CK, Su JC, Yu MC, Fang HY, Ann Surg Oncol 2012
27. Arsenic trioxide controls the fate of the PML-RARalpha oncoprotein by directly binding PML. Zhang XW, Yan XJ, Zhou ZR, Yang FF, Wu ZY, Sun HB, Liang WX, Song AX, Lallemand-Breitenbach V, Jeanne M, Zhang QY, Yang HY, Huang QH, Zhou GB, Tong JH, Zhang Y, Wu JH, Hu HY, De The H, Chen SJ, Chen Z, Science 2010 328 240 243 10.1126/science.1183424 20378816
28. Identification of cells initiating human melanomas. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, Fuhlbrigge RC, Kupper TS, Sayegh MH, Frank MH, Nature 2008 451 345 349 10.1038/nature06489 18202660
29. Inhibition by arsenic trioxide of human hepatoma cell growth. Oketani M, Kohara K, Tuvdendorj D, Ishitsuka K, Komorizono Y, Ishibashi K, Arima T, Cancer lett 2002 183 147 153 10.1016/S0304-3835(01)00800-X 12065089
30. Antitumor effect of arsenic trioxide in murine xenograft model. Kito M, Matsumoto K, Wada N, Sera K, Futatsugawa S, Naoe T, Nozawa Y, Akao Y, Cancer Sci 2003 94 1010 1014 10.1111/j.1349-7006.2003.tb01393.x 14611680
31. Arsenic trioxide in patients with hepatocellular carcinoma: a phase II trial. Lin CC, Hsu C, Hsu CH, Hsu WL, Cheng AL, Yang CH, Invest New Drugs 2007 25 77 84 16937079
32. A comparison of stem cell-related gene expression in the progenitor-rich limbal epithelium and the differentiating central corneal epithelium. Nieto-Miguel T, Calonge M, de la Mata A, Lopez-Paniagua M, Galindo S, de la Paz MF, Corrales RM, Mol Vis 2011 17 2102 2117 21850186
33. Mutations in Fbx4 inhibit dimerization of the SCF(Fbx4) ligase and contribute to cyclin D1 overexpression in human cancer. Barbash O, Zamfirova P, Lin DI, Chen X, Yang K, Nakagawa H, Lu F, Rustgi AK, Diehl JA, Cancer cell 2008 14 68 78 10.1016/j.ccr.2008.05.017 18598945
34. Induction of abnormal proliferation by nonmyelinating schwann cells triggers neurofibroma formation. Zheng H, Chang L, Patel N, Yang J, Lowe L, Burns DK, Zhu Y, Cancer cell 2008 13 117 128 10.1016/j.ccr.2008.01.002 18242512
35. ALDH1A isozymes are markers of human melanoma stem cells and potential therapeutic targets. Luo Y, Dallaglio K, Chen Y, Robinson WA, Robinson SE, McCarter MD, Wang J, Gonzalez R, Thompson DC, Norris DA, Roop DR, Vasiliou V, Fujita M, Stem Cells 2012 30 2100 2113 10.1002/stem.1193 22887839
36. Leukemia inhibitory factor-induced Stat3 signaling suppresses fibroblast growth factor 1-induced Erk1/2 activation to inhibit the downstream differentiation in mouse embryonic stem cells. Liu JW, Hsu YC, Kao CY, Su HL, Chiu IM, Stem Cells Dev 2013 22 1190 1197 10.1089/scd.2012.0229 23205673
37. Molecular pathways: induction of polyploidy as a novel differentiation therapy for leukemia. Krause DS, Crispino JD, Clin Cancer Res 2013 19 6084 6088 10.1158/1078-0432.CCR-12-2604 23963861
38. WNT signalling pathways as therapeutic targets in cancer. Anastas JN, Moon RT, Nat Rev Cancer 2012 13 11 26 10.1038/nrc3419
39. Arsenic trioxide-induced apoptosis and its enhancement by buthionine sulfoximine in hepatocellular carcinoma cell lines. Kito M, Akao Y, Ohishi N, Yagi K, Nozawa Y, Biochem Biophys Res Commun 2002 291 861 867 10.1006/bbrc.2002.6525 11866444
40. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1 + CD11b + myeloid cells that promote metastasis. Yang L, Huang J, Ren X, Gorska AE, Chytil A, Aakre M, Carbone DP, Matrisian LM, Richmond A, Lin PC, Moses HL, Cancer cell 2008 13 23 35 10.1016/j.ccr.2007.12.004 18167337
41. The Hedgehog's tale: developing strategies for targeting cancer. Ng JM, Curran T, Nat Rev Cancer 2011 11 493 501 10.1038/nrc3079 21614026
42. The EWS/FLI1 oncogenic transcription factor deregulates GLI1. Zwerner JP, Joo J, Warner KL, Christensen L, Hu-Lieskovan S, Triche TJ, May WA, Oncogene 2008 27 3282 3291 10.1038/sj.onc.1210991 18084326
43. GLI1 is a direct transcriptional target of EWS-FLI1 oncoprotein. Beauchamp E, Bulut G, Abaan O, Chen K, Merchant A, Matsui W, Endo Y, Rubin JS, Toretsky J, Uren A, J Biol Chem 2009 284 9074 9082 10.1074/jbc.M806233200 19189974
44. GLI1 is regulated through Smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation. Nolan-Stevaux O, Lau J, Truitt ML, Chu GC, Hebrok M, Fernandez-Zapico ME, Hanahan D, Genes Dev 2009 23 24 36 10.1101/gad.1753809 19136624
45. DACT3 is an epigenetic regulator of Wnt/beta-catenin signaling in colorectal cancer and is a therapeutic target of histone modifications. Jiang X, Tan J, Li J, Kivimae S, Yang X, Zhuang L, Lee PL, Chan MT, Stanton LW, Liu ET, Cheyette BN, Yu Q, Cancer cell 2008 13 529 541 10.1016/j.ccr.2008.04.019 18538736
46. Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. Levina V, Marrangoni AM, DeMarco R, Gorelik E, Lokshin AE, PloS one 2008 3 3077 10.1371/journal.pone.0003077 18728788
47. High-dose and long-term therapy with interferon-alfa inhibits tumor growth and recurrence in nude mice bearing human hepatocellular carcinoma xenografts with high metastatic potential. Wang L, Tang ZY, Qin LX, Wu XF, Sun HC, Xue Q, Ye SL, Hepatology 2000 32 43 48 10869287