Nuclear factor kappa B-mediated CD47 up-regulation promotes sorafenib resistance and its blockade synergizes the effect of sorafenib in hepatocellular carcinoma in mice

Hepatology

Volumn 62, Issue 2, 2015, Pages 534-545

  Lo, Jessica ^a,b   Lau, Eunice Yuen Ting ^a,b   Ching, Rachel Hiu Ha ^a,b   Cheng, Bowie Yik Ling ^a,b   Ma, Mark Kin Fai ^a,b   Ng, Irene Oi Lin ^a,b,c   Lee, Terence Kin Wah ^a,b  

^a THE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CD47 ANTIBODY; CD47 ANTIGEN; CELL ANTIBODY; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; PROTEIN KINASE B; SORAFENIB; UNCLASSIFIED DRUG; CARBANILAMIDE DERIVATIVE; CD47 PROTEIN, MOUSE; NICOTINAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CANCER CELL LINE; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; TUMOR XENOGRAFT; TUNEL ASSAY; UPREGULATION; XENOGRAFT; ANALOGS AND DERIVATIVES; ANIMAL; CARCINOMA, HEPATOCELLULAR; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENETICS; LIVER NEOPLASMS; METABOLISM; MOLECULARLY TARGETED THERAPY; RANDOMIZATION; SCID MOUSE; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; TUMOR CELL CULTURE;

ANIMALS; ANTIGENS, CD47; ANTINEOPLASTIC AGENTS; CARCINOMA, HEPATOCELLULAR; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; HUMANS; LIVER NEOPLASMS; MICE; MICE, SCID; MOLECULAR TARGETED THERAPY; NF-KAPPA B; NIACINAMIDE; PHENYLUREA COMPOUNDS; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; TUMOR CELLS, CULTURED; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84938203422     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27859     Document Type: Article

References (32)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics 2013. CA Cancer J Clin 2013;63:11-30.
2. Llovet JM, Di Bisceglie AM, Bruix J, Kramer BS, Lencioni R, Zhu AX, et al. Panel of Experts in HCC-Design Clinical Trials. Design and endpoints of clinical trials in hepatocellular carcinoma. J Natl Cancer Inst 2008;100:698-711.
3. 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.
4. Cheng AL, Kang YK, Chen Z, Tsao CJ, Qin S, Kim JS, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 2009;10:25-34.
5. Yau T, Yao TJ, Chan P, Wong H, Pang R, Fan ST, et al. The significance of early alpha-fetoprotein level changes in predicting clinical and survival benefits in advanced hepatocellular carcinoma patients receiving sorafenib. Oncologist 2011;16:1270-1279.
6. Villanueva A, Llovet JM. Second-line therapies in hepatocellular carcinoma: emergence of resistance to sorafenib. Clin Cancer Res 2012;18:1824-1826.
7. Shan J, Shen J, Liu L, Xia F, Xu C, Duan G, et al. Nanog regulates self-renewal of cancer stem cells through the insulin-like growth factor pathway in human hepatocellular carcinoma. Hepatology 2012;56:1004-1014.
8. Chen X, Lingala S, Khoobyari S, Nolta J, Zern MA, Wu J. Epithelial mesenchymal transition and hedgehog signaling activation are associated with chemoresistance and invasion of hepatoma subpopulations. J Hepatol 2011;55:838-845.
9. 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.
10. Yamashita T, Budhu A, Forgues M, Wang XW. Activation of hepatic stem cell marker EpCAM by Wnt-beta-catenin signaling in HCC. Cancer Res 2007;67:10831-20839.
11. 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.
12. Haraguchi N, Ishii H, Mimori K, Tanaka F, Ohkuma M, Kim HM, et al. CD13 is a therapeutic target in human liver cancer stem cells. J Clin Invest 2010;120:3326-3339.
13. Ma S, Lee TK, Zheng BJ, Chan KW, Guan XY. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008;27:1749-1758.
14. Lee TK, Castilho A, Cheung VC, Tang KH, Ma S, Ng IO. CD24+ liver tumor-initiating cells drive self-renewal and tumor initiation through Stat3-mediated nanog regulation. Cell Stem Cell 2011;9:50-63.
15. Wilson GS, Hu Z, Duan W, Tian A, Wang XM, McLeod D, et al. LCSCs Efficacy of using cancer stem cell markers in isolating and characterizing liver cancer stem cells. Stem Cells Dev 2013;22:2655-2664.
16. Xin HW, Ambe CM, Hari DM, Wiegand GW, Miller TC, Chen JQ, et al. Label-retaining liver cancer cells are relatively resistant to sorafenib. Gut 2013;62:1777-1786.
17. Lee TK, Cheung VC, Lu P, Lau EY, Ma S, Tang KH, et al. Blockade of CD47 mediated CTSS-PAR2 signaling provides a therapeutic target for hepatocellular carcinoma. Hepatology 2014;60:179-191.
18. Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, Gibbs KD, Jr., et al. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 2009;138:286-299.
19. Chan KS, Espinosa I, Chao M, Wong D, Ailles L, Diehn M, et al. Identification, molecular characterization, clinicalprognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc Natl Acad Sci U S A 2009;106:14016-14021.
20. Willingham SB, Volkmer JP, Gentles AJ, Sahoo D, Dalerba P, Mitra SS, et al. The CD47-signal regulatory protein alpha (SIPRα) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci U S A 2012;109:6662-6667.
21. Tseng D, Volkmer JP, Willingham SB, Contreras-Trujillo H, Fathman JW, Fernhoff NB, et al. Anti-CD47 antibody-mediated phagocytosis of cancer by macrophage primes an effective antitumor T-cell response. Proc Natl Acad Sci U S A 2013;110:11103-11108.
22. Schmitz ML, Mattioli I, Buss H, Kracht M. NF-kappaB: a multifaceted transcription factor regulated at several levels. Chembiochem 2004;5:1348-1358.
23. Yamashita T, Forgues M, Wang W, Kim JW, Ye Q, Jia H, et al. EpCAM and alpha-fetoprotein expression defines novel prognostic subtypes of hepatocellular carcinoma. Cancer Res 2008;68:1451-1461.
24. Zhai B, Hu F, Jiang X, Xu J, Zhao D, Liu B, et al. Inhibition of akt reverses the acquired resistance to sorafenib by switching protective autophagy to autophagic cell death in hepatocellular carcinoma. Mol Cancer Ther 2014;13:1589-1598.
25. Chow AK, Ng L, Lam CS, Wong SK, Wan TM, Cheng NS, et al. The Enhanced metastatic potential of hepatocellular carcinoma (HCC) cells with sorafenib resistance. PLoS One 2013;8:e78675.
26. Xin HW, Ambe CM, Hari DM, Wiegand GW, Miller TC, Chen JQ, et al. Label-retaining liver cancer cells are relatively resistant to sorafenib. Gut 2013;62:1777-1786.
27. Chang WT, Huang AM. Alpha-Pal/NRF-1 regulates the promoter of the human integrin-associated protein/CD47 gene. J Biol Chem 2004;279:14542-14550.
28. Liu P, Kimmoun E, Legrand A, Sauvanet A, Degott C, Lardeux B, et al. Activation of NF-kappa B, AP-1 and STAT transcription factors is a frequent and early event in human hepatocellular carcinomas. J Hepatol 2002;37:63-71.
29. Kuo HP, Wang Z, Lee DF, Iwasaki M, Duque-Afonso J, Wong SH, et al. Epigenetic roles of MLL oncoproteins are dependent on NF-κB. Cancer Cell 2013;24:423-437.
30. Yamamoto M, Taguchi Y, Ito-Kureha T, Semba K, Yamaguchi N, Inoue J. NF-κB non-cell-autonomously regulates cancer stem cell populations in the basal-like breast cancer subtype. Nat Commun 2013;4:2299.
31. Rausch V, Liu L, Kallifatidis G, Baumann B, Mattern J, Gladkich J, et al. Synergistic activity of sorafenib and sulforaphane abolishes pancreatic cancer stem cell characteristics. Cancer Res 2010;70:5004-5013.
32. Maxhimer JB, Soto-Pantoja DR, Ridnour LA, Shih HB, Degraff WG, Tsokos M, et al. Radioprotection in normal tissue and delayed tumor growth by blockade of CD47 signaling. Sci Transl Med 2009;1:3ra7.