Promotion of cancer stem-like cell properties in hepatitis C virus-infected hepatocytes

Journal of Virology

Volumn 89, Issue 22, 2015, Pages 11549-11556

  Kwon, Young Chan ^a   Bose, Sandip K ^a   Steele, Robert ^a   Meyer, Keith ^a   Di Bisceglie, Adrian M ^a   Ray, Ratna B ^a   Ray, Ranjit ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; CORE PROTEIN; DASATINIB; IMATINIB; MESSENGER RNA; NOTCH1 RECEPTOR; PROTEIN INHIBITOR; SORAFENIB; STATTIC; STEM CELL FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; VIMENTIN; CARBANILAMIDE DERIVATIVE; NICOTINAMIDE; STAT3 PROTEIN; STAT3 PROTEIN, HUMAN; STEM CELL FACTOR RECEPTOR; SULFOXIDE; TUMOR MARKER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER STEM CELL; CARCINOGENICITY; CELL CULTURE; CELL DEATH; CELL GROWTH; CELL TRANSFORMATION; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; HEPATITIS C; HEPATITIS C VIRUS SUBTYPE 2A; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER BIOPSY; LIVER CELL; MOUSE; NOD SCID GAMMA MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; TUMOR GROWTH; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER TRANSPLANTATION; CYTOLOGY; DRUG EFFECTS; GENETICS; HEPACIVIRUS; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; MULTICELLULAR SPHEROID; PATHOLOGY; TUMOR CELL CULTURE; VIROLOGY; XENOGRAFT;

ANIMALS; BIOMARKERS, TUMOR; CARCINOMA, HEPATOCELLULAR; CYCLIC S-OXIDES; DASATINIB; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HUMANS; IMATINIB MESYLATE; LIVER NEOPLASMS; MICE; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; NIACINAMIDE; PHENYLUREA COMPOUNDS; PROTO-ONCOGENE PROTEINS C-KIT; RNA, MESSENGER; SPHEROIDS, CELLULAR; STAT3 TRANSCRIPTION FACTOR; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 84945939028     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01946-15     Document Type: Article

References (45)

1. Arzumanyan A, Reis HM, Feitelson MA. 2013. Pathogenic mechanisms in HBV-and HCV-associated hepatocellular carcinoma. Nat Rev Cancer 13:123-135. http://dx.doi.org/10.1038/nrc3449.
2. Banerjee A, Ray RB, Ray R. 2010. Oncogenic potential of hepatitis C virus proteins. Viruses 2:2108-2133. http://dx.doi.org/10.3390/v2092108.
3. Kwon YC, Ray RB, Ray R. 2014. Hepatitis C virus infection: establishment of chronicity and liver disease progression. EXCLI J 13:977-996.
4. Everson GT, Hoefs JC, SeeffLB, Bonkovsky HL, Naishadham D, Shiffman ML, Kahn JA, Lok AS, Di Bisceglie AM, Lee WM, Dienstag JL, Ghany MG, Morishima C, HALT-C Trial Group. 2006. Impact of disease severity on outcome of antiviral therapy for chronic hepatitis C: lessons from the HALT-C trial. Hepatology 44:1675-1684. http://dx.doi.org/10.1002/hep.21440.
5. van der Meer AJ, Veldt BJ, Feld JJ, Wedemeyer H, Dufour JF, Lammert F, Duarte-Rojo A, Heathcote EJ, Manns MP, Kuske L, Zeuzem S, Hofmann WP, de Knegt RJ, Hansen BE, Janssen HL. 2012. Association between sustained virological response and all-cause mortality among patients with chronic hepatitis C and advanced hepatic fibrosis. JAMA 308: 2584-2593. http://dx.doi.org/10.1001/jama.2012.144878.
6. Hoshida Y, Fuchs BC, Bardeesy N, Baumert TF, Chung RT. 2014. Pathogenesis and prevention of hepatitis C virus-induced hepatocellular carcinoma. J Hepatol 61:S79-S90. http://dx.doi.org/10.1016/j.jhep.2014.07.010.
7. Obokata H, Sasai Y, Niwa H, Kadota M, Andrabi M, Takata N, Tokoro M, Terashita Y, Yonemura S, Vacanti CA, Wakayama T. 2014. Bidirectional developmental potential in reprogrammed cells with acquired pluripotency. Nature 505:676-680. http://dx.doi.org/10.1038/nature12969.
8. Obokata H, Wakayama T, Sasai Y, Kojima K, Vacanti MP, Niwa H, Yamato M, Vacanti CA. 2014. Stimulus-triggered fate conversion of somatic cells into pluripotency. Nature 505:641-647. http://dx.doi.org/10.1038/nature12968.
9. Bose SK, Meyer K, Di Bisceglie AM, Ray RB, Ray R. 2012. Hepatitis C virus induces epithelial-mesenchymal transition in primary human hepatocytes. J Virol 86:13621-13628. http://dx.doi.org/10.1128/JVI.02016-12.
10. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. 2008. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133:704-715. http://dx.doi.org/10.1016/j.cell.2008.03.027.
11. Mishra L, Banker T, Murray J, Byers S, Thenappan A, He AR, Shetty K, Johnson L, Reddy EP. 2009. Liver stem cells and hepatocellular carcinoma. Hepatology 49:318-329. http://dx.doi.org/10.1002/hep.22704.
12. Rountree CB, Mishra L, Willenbring H. 2012. Stem cells in liver diseases and cancer: recent advances on the path to new therapies. Hepatology 55:298-306. http://dx.doi.org/10.1002/hep.24762.
13. Thiery JP, Acloque H, Huang RY, Nieto MA. 2009. Epithelialmesenchymal transitions in development and disease. Cell 139:871-890. http://dx.doi.org/10.1016/j.cell.2009.11.007.
14. Yang J, Weinberg RA. 2008. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14:818-829. http://dx.doi.org/10.1016/j.devcel.2008.05.009.
15. Banerjee A, Mazumdar B, Meyer K, Di Bisceglie AM, Ray RB, Ray R. 2011. Transcriptional repression of C4 complement by hepatitis C virus proteins. J Virol 85:4157-4166. http://dx.doi.org/10.1128/JVI.02449-10.
16. Basu A, Meyer K, Ray RB, Ray R. 2002. Hepatitis C virus core protein is necessary for the maintenance of immortalized human hepatocytes. Virology 298:53-62. http://dx.doi.org/10.1006/viro.2002.1460.
17. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY, Bapat SA. 2009. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 27:2059-2068. http://dx.doi.org/10.1002/stem.154.
18. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. 2008. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 3:e2888. http://dx.doi.org/10.1371/journal.pone.0002888.
19. Santisteban M, Reiman JM, Asiedu MK, Behrens MD, Nassar A, Kalli KR, Haluska P, Ingle JN, Hartmann LC, Manjili MH, Radisky DC, Ferrone S, Knutson KL. 2009. Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res 69: 2887-2895. http://dx.doi.org/10.1158/0008-5472.CAN-08-3343.
20. Broudy VC. 1997. Stem cell factor and hematopoiesis. Blood 90:1345-1364.
21. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R, Young RA. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947-956. http://dx.doi.org/10.1016/j.cell.2005.08.020.
22. Villanueva A, Alsinet C, Yanger K, Hoshida Y, Zong Y, Toffanin S, Rodriguez-Carunchio L, Sole M, Thung S, Stanger BZ, Llovet JM. 2012. Notch signaling is activated in human hepatocellular carcinoma and induces tumor formation in mice. Gastroenterology 143:1660-1669 e1667. http://dx.doi.org/10.1053/j.gastro.2012.09.002.
23. Takebe N, Harris PJ, Warren RQ, Ivy SP. 2011. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol 8:97-106. http://dx.doi.org/10.1038/nrclinonc.2010.196.
24. Mazumdar B, Kim H, Meyer K, Bose SK, Di Bisceglie AM, Ray RB, Ray R. 2012. Hepatitis C virus proteins inhibit C3 complement production. J Virol 86:2221-2228. http://dx.doi.org/10.1128/JVI.06577-11.
25. Akkari L, Gregoire D, Floc'h N, Moreau M, Hernandez C, Simonin Y, Rosenberg AR, Lassus P, Hibner U. 2012. Hepatitis C viral protein NS5A induces EMT and participates in oncogenic transformation of primary hepatocyte precursors. J Hepatol 57:1021-1028. http://dx.doi.org/10.1016/j.jhep.2012.06.027.
26. Quan H, Zhou F, Nie D, Chen Q, Cai X, Shan X, Zhou Z, Chen K, Huang A, Li S, Tang N. 2014. Hepatitis C virus core protein epigenetically silences SFRP1 and enhances HCC aggressiveness by inducing epithelial-mesenchymal transition. Oncogene 33:2826-2835. http://dx.doi.org/10.1038/onc.2013.225.
27. Maeda K, Nishiyama C, Ogawa H, Okumura K. 2010. GATA2 and Sp1 positively regulate the c-kit promoter in mast cells. J Immunol 185:4252-4260. http://dx.doi.org/10.4049/jimmunol.1001228.
28. Iqbal J, McRae S, Banaudha K, Mai T, Waris G. 2013. Mechanism of hepatitis C virus (HCV)-induced osteopontin and its role in epithelial to mesenchymal transition of hepatocytes. J Biol Chem 288:36994-37009. http://dx.doi.org/10.1074/jbc. M113.492314.
29. Mazumdar B, Kim H, Meyer K, Bose SK, Di Bisceglie AM, Ray RB, Diamond MS, Atkinson JP, Ray R. 2013. Hepatitis C virus infection upregulates CD55 expression on the hepatocyte surface and promotes association with virus particles. J Virol 87:7902-7910. http://dx.doi.org/10.1128/JVI.00917-13.
30. Levina V, Marrangoni A, Wang T, Parikh S, Su Y, Herberman R, Lokshin A, Gorelik E. 2010. Elimination of human lung cancer stem cells through targeting of the stem cell factor-c-kit autocrine signaling loop. Cancer Res 70:338-346. http://dx.doi.org/10.1158/0008-5472.CAN-09-1102.
31. Liu CY, Tseng LM, Su JC, Chang KC, Chu PY, Tai WT, Shiau CW, Chen KF. 2013. Novel sorafenib analogues induce apoptosis through SHP-1 dependent STAT3 inactivation in human breast cancer cells. Breast Cancer Res 15:R63. http://dx.doi.org/10.1186/bcr3457.
32. Bhattacharya S, Ray RM, Johnson LR. 2005. STAT3-mediated transcription of Bcl-2, Mcl-1 and c-IAP2 prevents apoptosis in polyamine-depleted cells. Biochem J 392:335-344. http://dx.doi.org/10.1042/BJ20050465.
33. Cheng M, Qin G. 2012. Progenitor cell mobilization and recruitment: SDF-1, CXCR4, alpha4-integrin, and c-kit. Prog Mol Biol Transl Sci 111:243-264. http://dx.doi.org/10.1016/B978-0-12-398459-3.00011-3.
34. Hassan HT. 2009. c-Kit expression in human normal and malignant stem cells prognostic and therapeutic implications. Leuk Res 33:5-10. http://dx.doi.org/10.1016/j.leukres.2008.06.011.
35. Mansuroglu T, Baumhoer D, Dudas J, Haller F, Cameron S, Lorf T, Fuzesi L, Ramadori G. 2009. Expression of stem cell factor receptor c-kit in human nontumoral and tumoral hepatic cells. Eur J Gastroenterol Hepatol 21:1206-1211. http://dx.doi.org/10.1097/MEG.0b013e328317f4ef.
36. Ronnstrand L. 2004. Signal transduction via the stem cell factor receptor/c-Kit. Cell Mol Life Sci 61:2535-2548. http://dx.doi.org/10.1007/s00018-004-4189-6.
37. Tarn C, Skorobogatko YV, Taguchi T, Eisenberg B, von Mehren M, Godwin AK. 2006. Therapeutic effect of imatinib in gastrointestinal stromal tumors: AKT signaling dependent and independent mechanisms. Cancer Res 66:5477-5486. http://dx.doi.org/10.1158/0008-5472.CAN-05-3906.
38. Shaw TJ, Vanderhyden BC. 2007. AKT mediates the pro-survival effects of KIT in ovarian cancer cells and is a determinant of sensitivity to imatinib mesylate. Gynecol Oncol 105:122-131. http://dx.doi.org/10.1016/j.ygyno.2006.10.052.
39. Krug LM, Crapanzano JP, Azzoli CG, Miller VA, Rizvi N, Gomez J, Kris MG, Pizzo B, Tyson L, Dunne M, Heelan RT. 2005. Imatinib mesylate lacks activity in small cell lung carcinoma expressing c-kit protein: a phase II clinical trial. Cancer 103:2128-2131. http://dx.doi.org/10.1002/cncr.21000.
40. Alberts DS, Liu PY, Wilczynski SP, Jang A, Moon J, Ward JH, Beck JT, Clouser M, Markman M. 2007. Phase II trial of imatinib mesylate in recurrent, biomarker positive, ovarian cancer (Southwest Oncology Group protocol S0211). Int J Gynecol Cancer 17:784-788. http://dx.doi.org/10.1111/j.1525-1438.2007.00882.x.
41. Cristofanilli M, Morandi P, Krishnamurthy S, Reuben JM, Lee BN, Francis D, Booser DJ, Green MC, Arun BK, Pusztai L, Lopez A, Islam R, Valero V, Hortobagyi GN. 2008. Imatinib mesylate (Gleevec) in advanced breast cancer-expressing C-Kit or PDGFR-beta: clinical activity and biological correlations. Ann Oncol 19:1713-1719. http://dx.doi.org/10.1093/annonc/mdn352.
42. Schust J, Sperl B, Hollis A, Mayer TU, Berg T. 2006. Stattic: a smallmolecule inhibitor of STAT3 activation and dimerization. Chem Biol 13: 1235-1242. http://dx.doi.org/10.1016/j.chembiol.2006.09.018.
43. Liu S, Cong Y, Wang D, Sun Y, Deng L, Liu Y, Martin-Trevino R, Shang L, McDermott SP, Landis MD, Hong S, Adams A, D'Angelo R, Ginestier C, Charafe-Jauffret E, Clouthier SG, Birnbaum D, Wong ST, Zhan M, Chang JC, Wicha MS. 2014. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Rep 2:78-91. http://dx.doi.org/10.1016/j.stemcr.2013.11.009.
44. Broxterman HJ, Georgopapadakou NH. 2007. Anticancer therapeutics: a surge of new developments increasingly target tumor and stroma. Drug Resist Updat 10:182-193. http://dx.doi.org/10.1016/j.drup.2007.07.001.
45. LoPiccolo J, Blumenthal GM, Bernstein WB, Dennis PA. 2008. Targeting the PI3K/Akt/mTOR pathway: effective combinations and clinical considerations. Drug Resist Updat 11:32-50. http://dx.doi.org/10.1016/j.drup.2007.11.003.