Inflammation and liver tumorigenesis

Beicheng Sun, Michael Karin

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Front. Med. ›› 2013, Vol. 7 ›› Issue (2) : 242-254. DOI: 10.1007/s11684-013-0256-4
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Inflammation and liver tumorigenesis

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Abstract

Inflammation has been considered as one of the hallmarks of cancer, and chronic hepatitis is a major cause of liver cancer. This review will focus on the pathogenic role of inflammation in hepatocarcinogenesis and will discuss recent advances in understanding the chronic hepatitis-liver cancer link based on hot spots in liver cancer research, including cellular interaction, cytokines, microRNA and stem cells. All of these mechanisms should be taken into consideration because they are crucial for the development of more efficacious therapeutic strategies for preventing and treating human chronic hepatitis and hepatocellular carcinoma.

Keywords

hepatocellular carcinoma / hepatitis / cytokine / stem cell / miRNA

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Beicheng Sun, Michael Karin. Inflammation and liver tumorigenesis. Front Med, 2013, 7(2): 242‒254 https://doi.org/10.1007/s11684-013-0256-4

References

[1]
Whiteside TL. The tumor microenvironment and its role in promoting tumor growth. Oncogene2008; 27(45): 5904-5912
CrossRef Pubmed Google scholar
[2]
Hoshida Y, Villanueva A, Kobayashi M, Peix J, Chiang DY, Camargo A, Gupta S, Moore J, Wrobel MJ, Lerner J, Reich M, Chan JA, Glickman JN, Ikeda K, Hashimoto M, Watanabe G, Daidone MG, Roayaie S, Schwartz M, Thung S, Salvesen HB, Gabriel S, Mazzaferro V, Bruix J, Friedman SL, Kumada H, Llovet JM, Golub TR. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med2008; 359(19): 1995-2004
CrossRef Pubmed Google scholar
[3]
Levrero M. Viral hepatitis and liver cancer: the case of hepatitis C. Oncogene2006; 25(27): 3834-3847
CrossRef Pubmed Google scholar
[4]
Sweet MJ, Hume DA. Endotoxin signal transduction in macrophages. J Leukoc Biol1996; 60(1): 8-26
Pubmed
[5]
Yan S, Wang L, Liu N, Wang Y, Chu Y. Critical role of interleukin-17/interleukin-17 receptor axis in mediating Con A-induced hepatitis. Immunol Cell Biol2012; 90(4): 421-428
Pubmed
[6]
Hsieh WT, Tsai CT, Wu JB, Hsiao HB, Yang LC, Lin WC. Kinsenoside, a high yielding constituent from Anoectochilus formosanus, inhibits carbon tetrachloride induced Kupffer cells mediated liver damage. J Ethnopharmacol2011; 135(2): 440-449
CrossRef Pubmed Google scholar
[7]
Ramaiah SK, Jaeschke H. Role of neutrophils in the pathogenesis of acute inflammatory liver injury. Toxicol Pathol2007; 35(6): 757-766
CrossRef Pubmed Google scholar
[8]
Jaeschke H, Hasegawa T. Role of neutrophils in acute inflammatory liver injury. Liver Int2006; 26(8): 912-919
CrossRef Pubmed Google scholar
[9]
Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol1991; 260(3 Pt 1): G355-G362
Pubmed
[10]
Lee WM. Acetaminophen and the U.S. Acute Liver Failure Study Group: lowering the risks of hepatic failure. Hepatology2004; 40(1): 6-9
CrossRef Pubmed Google scholar
[11]
Knolle PA, Gerken G. Local control of the immune response in the liver. Immunol Rev2000;174:21-34
Pubmed
[12]
Ishida Y, Kondo T, Ohshima T, Fujiwara H, Iwakura Y, Mukaida N. A pivotal involvement of IFN-gamma in the pathogenesis of acetaminophen-induced acute liver injury. FASEB J2002; 16(10): 1227-1236
CrossRef Pubmed Google scholar
[13]
Liu ZX, Govindarajan S, Kaplowitz N. Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity. Gastroenterology2004; 127(6): 1760-1774
CrossRef Pubmed Google scholar
[14]
Arshad MI, Rauch M, L’helgoualc’h A, Julia V, Leite-de-Moraes MC, Lucas-Clerc C, Piquet-Pellorce C, Samson M. NKT cells are required to induce high IL-33 expression in hepatocytes during ConA-induced acute hepatitis. Eur J Immunol2011; 41(8): 2341-2348
CrossRef Pubmed Google scholar
[15]
Bissell DM, Wang SS, Jarnagin WR, Roll FJ. Cell-specific expression of transforming growth factor-beta in rat liver. Evidence for autocrine regulation of hepatocyte proliferation. J Clin Invest1995; 96(1): 447-455
CrossRef Pubmed Google scholar
[16]
Knolle PA, Löser E, Protzer U, Duchmann R, Schmitt E, zum Büschenfelde KH, Rose-John S, Gerken G. Regulation of endotoxin-induced IL-6 production in liver sinusoidal endothelial cells and Kupffer cells by IL-10. Clin Exp Immunol1997; 107(3): 555-561
CrossRef Pubmed Google scholar
[17]
Knolle PA, Germann T, Treichel U, Uhrig A, Schmitt E, Hegenbarth S, Lohse AW, Gerken G. Endotoxin down-regulates T cell activation by antigen-presenting liver sinusoidal endothelial cells. J Immunol1999; 162(3): 1401-1407
Pubmed
[18]
Knolle PA, Limmer A. Neighborhood politics: the immunoregulatory function of organ-resident liver endothelial cells. Trends Immunol2001; 22(8): 432-437
CrossRef Pubmed Google scholar
[19]
Knolle PA, Uhrig A, Hegenbarth S, Löser E, Schmitt E, Gerken G, Lohse AW. IL-10 down-regulates T cell activation by antigen-presenting liver sinusoidal endothelial cells through decreased antigen uptake via the mannose receptor and lowered surface expression of accessory molecules. Clin Exp Immunol1998; 114(3): 427-433
CrossRef Pubmed Google scholar
[20]
Crispe IN. The liver as a lymphoid organ. Annu Rev Immunol2009; 27: 147-163
Pubmed
[21]
Kojima N, Sato M, Suzuki A, Sato T, Satoh S, Kato T, Senoo H. Enhanced expression of B7-1, B7-2, and intercellular adhesion molecule 1 in sinusoidal endothelial cells by warm ischemia/reperfusion injury in rat liver. Hepatology2001; 34(4): 751-757
CrossRef Pubmed Google scholar
[22]
Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, Sahgal N, Hussell T, Feldmann M, Udalova IA. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol2011; 12(3): 231-238
CrossRef Pubmed Google scholar
[23]
Chappell L, Kaiser P, Barrow P, Jones MA, Johnston C, Wigley P. The immunobiology of avian systemic salmonellosis. Vet Immunol Immunopathol2009; 128(1-3): 53-59
CrossRef Pubmed Google scholar
[24]
Larrubia JR, Benito-Martínez S, Calvino M, Sanz-de-Villalobos E, Parra-Cid T. Role of chemokines and their receptors in viral persistence and liver damage during chronic hepatitis C virus infection. World J Gastroenterol2008; 14(47): 7149-7159
CrossRef Pubmed Google scholar
[25]
Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol2008; 214(2): 199-210
CrossRef Pubmed Google scholar
[26]
Movahedi K, Laoui D, Gysemans C, Baeten M, Stangé G, Van den Bossche J, Mack M, Pipeleers D, In’t Veld P, De Baetselier P, Van Ginderachter JA. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res2010; 70(14): 5728-5739
CrossRef Pubmed Google scholar
[27]
Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol2010; 11(10): 889-896
CrossRef Pubmed Google scholar
[28]
Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell2010; 140(6): 883-899
CrossRef Pubmed Google scholar
[29]
Karin M. Nuclear factor-kappaB in cancer development and progression. Nature2006; 441(7092): 431-436
CrossRef Pubmed Google scholar
[30]
Zamarron BF, Chen W. Dual roles of immune cells and their factors in cancer development and progression. Int J Biol Sci2011; 7(5): 651-658
CrossRef Pubmed Google scholar
[31]
Chen S, Akbar SM, Abe M, Hiasa Y, Onji M. Immunosuppressive functions of hepatic myeloid-derived suppressor cells of normal mice and in a murine model of chronic hepatitis B virus. Clin Exp Immunol2011; 166(1): 134-142
CrossRef Pubmed Google scholar
[32]
Hu CE, Gan J, Zhang RD, Cheng YR, Huang GJ. Up-regulated myeloid-derived suppressor cell contributes to hepatocellular carcinoma development by impairing dendritic cell function. Scand J Gastroenterol2011; 46(2): 156-164
CrossRef Pubmed Google scholar
[33]
Hoechst B, Ormandy LA, Ballmaier M, Lehner F, Krüger C, Manns MP, Greten TF, Korangy F. A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology2008; 135(1): 234-243
CrossRef Pubmed Google scholar
[34]
Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, Lehner F, Manns MP, Greten TF, Korangy F. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology2009; 50(3): 799-807
CrossRef Pubmed Google scholar
[35]
Grivennikov SI, Karin M. Inflammation and oncogenesis: a vicious connection. Curr Opin Genet Dev2010; 20(1): 65-71
CrossRef Pubmed Google scholar
[36]
Voloboueva LA, Giffard RG. Inflammation, mitochondria, and the inhibition of adult neurogenesis. J Neurosci Res2011; 89(12): 1989-1996
CrossRef Pubmed Google scholar
[37]
Tawara K, Oxford JT, Jorcyk CL. Clinical significance of interleukin (IL)-6 in cancer metastasis to bone: potential of anti-IL-6 therapies. Cancer Manag Res2011;3:177-189
Pubmed
[38]
Tanaka T, Narazaki M, Kishimoto T. Therapeutic Targeting of the Interleukin-6 Receptor. Annu Rev Pharmacol Toxicol2012; 52: 199-219
Pubmed
[39]
Mair M, Blaas L, Osterreicher CH, Casanova E, Eferl R. JAK-STAT signaling in hepatic fibrosis. Front Biosci2011; 17: 2794-2811
Pubmed
[40]
Jones SA, Scheller J, Rose-John S. Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. J Clin Invest2011; 121(9): 3375-3383
CrossRef Pubmed Google scholar
[41]
Erreni M, Mantovani A, Allavena P. Tumor-associated macrophages (TAM) and inflammation in colorectal cancer. Cancer Microenviron2011; 4(2): 141-154
CrossRef Pubmed Google scholar
[42]
Wang YC, Xu GL, Jia WD, Han SJ, Ren WH, Wang W, Liu WB, Zhang CH, Chen H. Estrogen suppresses metastasis in rat hepatocellular carcinoma through decreasing interleukin-6 and hepatocyte growth factor expression. Inflammation2012; 35(1): 143-149
Pubmed
[43]
Jiang R, Deng L, Zhao L, Li X, Zhang F, Xia Y, Gao Y, Wang X, Sun B. miR-22 promotes HBV-related hepatocellular carcinoma development in males. Clin Cancer Res2011; 17(17): 5593-5603
CrossRef Pubmed Google scholar
[44]
Hsu SH, Wang LT, Lee KT, Chen YL, Liu KY, Suen JL, Chai CY, Wang SN. Pro-inflammatory homeobox gene, ISX, regulates tumor growth and survival in hepatocellular carcinoma. Cancer Res Cancer Res2013; 73(2): 508-518
Pubmed
[45]
Kroy DC, Beraza N, Tschaharganeh DF, Sander LE, Erschfeld S, Giebeler A, Liedtke C, Wasmuth HE, Trautwein C, Streetz KL. Lack of interleukin-6/glycoprotein 130/signal transducers and activators of transcription-3 signaling in hepatocytes predisposes to liver steatosis and injury in mice. Hepatology2010; 51(2): 463-473
CrossRef Pubmed Google scholar
[46]
Ando M, Uehara I, Kogure K, Asano Y, Nakajima W, Abe Y, Kawauchi K, Tanaka N. Interleukin 6 enhances glycolysis through expression of the glycolytic enzymes hexokinase 2 and 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3. J Nippon Med Sch2010; 77(2): 97-105
CrossRef Pubmed Google scholar
[47]
Liu Y, Li PK, Li C, Lin J. Inhibition of STAT3 signaling blocks the anti-apoptotic activity of IL-6 in human liver cancer cells. J Biol Chem2010; 285(35): 27429-27439
CrossRef Pubmed Google scholar
[48]
Alison MR, Nicholson LJ, Lin WR. Chronic inflammation and hepatocellular carcinoma. Recent Results Cancer Res2011; 185: 135-148
Pubmed
[49]
Sander LE, Sackett SD, Dierssen U, Beraza N, Linke RP, Müller M, Blander JM, Tacke F, Trautwein C. Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J Exp Med2010; 207(7): 1453-1464
CrossRef Pubmed Google scholar
[50]
Kushibiki S. Tumor necrosis factor-α-induced inflammatory responses in cattle. Anim Sci J2011; 82(4): 504-511
CrossRef Pubmed Google scholar
[51]
Caminero A, Comabella M, Montalban X. Tumor necrosis factor alpha (TNF-α), anti-TNF-α and demyelination revisited: an ongoing story. J Neuroimmunol2011; 234(1-2): 1-6
CrossRef Pubmed Google scholar
[52]
Shukla R, Yue J, Siouda M, Gheit T, Hantz O, Merle P, Zoulim F, Krutovskikh V, Tommasino M, Sylla BS. Proinflammatory cytokine TNF-α increases the stability of hepatitis B virus X protein through NF-κB signaling. Carcinogenesis2011; 32(7): 978-985
CrossRef Pubmed Google scholar
[53]
Shi Z, Du C. Tumor necrosis factor alpha 308 G/A polymorphism and hepatocellular carcinoma risk in a Chinese population. Genet Test Mol Biomarkers2011; 15(7-8): 569-572
CrossRef Pubmed Google scholar
[54]
Wang B, Wang J, Zheng Y, Zhou S, Zheng J, Wang F, Ma X, Zeng Z. A study of TNF-alpha-238 and-308 polymorphisms with different outcomes of persistent hepatitis B virus infection in China. Pathology2010; 42(7): 674-680
CrossRef Pubmed Google scholar
[55]
Chen KF, Tai WT, Liu TH, Huang HP, Lin YC, Shiau CW, Li PK, Chen PJ, Cheng AL. Sorafenib overcomes TRAIL resistance of hepatocellular carcinoma cells through the inhibition of STAT3. Clin Cancer Res2010; 16(21): 5189-5199
CrossRef Pubmed Google scholar
[56]
Xia L, Mo P, Huang W, Zhang L, Wang Y, Zhu H, Tian D, Liu J, Chen Z, Zhang Y, Chen Z, Hu H, Fan D, Nie Y, Wu K. The TNF-α/ROS/HIF-1-induced upregulation of FoxMI expression promotes HCC proliferation and resistance to apoptosis. Carcinogenesis2012; 33(11): 2250-2259
CrossRef Pubmed Google scholar
[57]
Muntané J. Targeting cell death and survival receptors in hepatocellular carcinoma. Anticancer Agents Med Chem2011; 11(6): 576-584
CrossRef Pubmed Google scholar
[58]
Kriegl L, Jung A, Engel J, Jackstadt R, Gerbes AL, Gallmeier E, Reiche JA, Hermeking H, Rizzani A, Bruns CJ, Kolligs FT, Kirchner T, Göke B, De Toni EN. Expression, cellular distribution, and prognostic relevance of TRAIL receptors in hepatocellular carcinoma. Clin Cancer Res2010; 16(22): 5529-5538
CrossRef Pubmed Google scholar
[59]
Giannelli G, Mazzocca A, Fransvea E, Lahn M, Antonaci S. Inhibiting TGF-β signaling in hepatocellular carcinoma. Biochim Biophys Acta2011; 1815(2): 214-223
Pubmed
[60]
Achyut BR, Yang L. Transforming growth factor-β in the gastrointestinal and hepatic tumor microenvironment. Gastroenterology2011; 141(4): 1167-1178
CrossRef Pubmed Google scholar
[61]
Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol2006; 7(2): 131-142
CrossRef Pubmed Google scholar
[62]
Coulouarn C, Factor VM, Thorgeirsson SS. Transforming growth factor-beta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer. Hepatology2008; 47(6): 2059-2067
CrossRef Pubmed Google scholar
[63]
Mamiya T, Yamazaki K, Masugi Y, Mori T, Effendi K, Du W, Hibi T, Tanabe M, Ueda M, Takayama T, Sakamoto M. Reduced transforming growth factor-beta receptor II expression in hepatocellular carcinoma correlates with intrahepatic metastasis. Lab Invest2010; 90(9): 1339-1345
CrossRef Pubmed Google scholar
[64]
Ito N, Kawata S, Tamura S, Shirai Y, Kiso S, Tsushima H, Matsuzawa Y. Positive correlation of plasma transforming growth factor-beta 1 levels with tumor vascularity in hepatocellular carcinoma. Cancer Lett1995; 89(1): 45-48
CrossRef Pubmed Google scholar
[65]
Mazzocca A, Fransvea E, Lavezzari G, Antonaci S, Giannelli G. Inhibition of transforming growth factor beta receptor I kinase blocks hepatocellular carcinoma growth through neo-angiogenesis regulation. Hepatology2009; 50(4): 1140-1151
CrossRef Pubmed Google scholar
[66]
Wu K, Ding J, Chen C, Sun W, Ning BF, Wen W, Huang L, Han T, Yang W, Wang C, Li Z, Wu MC, Feng GS, Xie WF, Wang HY. Hepatic transforming growth factor beta gives rise to tumor-initiating cells and promotes liver cancer development. Hepatology2012; 56(6): 2255-2267
CrossRef Pubmed Google scholar
[67]
Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol2005; 6(11): 1133-1141
CrossRef Pubmed Google scholar
[68]
Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol2007; 25: 821-852
Pubmed
[69]
Kolls JK, Lindén A. Interleukin-17 family members and inflammation. Immunity2004; 21(4): 467-476
CrossRef Pubmed Google scholar
[70]
Dong C. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol2008; 8(5): 337-348
CrossRef Pubmed Google scholar
[71]
Volpe E, Servant N, Zollinger R, Bogiatzi SI, Hupé P, Barillot E, Soumelis V. A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses. Nat Immunol2008; 9(6): 650-657
CrossRef Pubmed Google scholar
[72]
Manel N, Unutmaz D, Littman DR. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol2008; 9(6): 641-649
CrossRef Pubmed Google scholar
[73]
Notley CA, Inglis JJ, Alzabin S, McCann FE, McNamee KE, Williams RO. Blockade of tumor necrosis factor in collagen-induced arthritis reveals a novel immunoregulatory pathway for Th1 and Th17 cells. J Exp Med2008; 205(11): 2491-2497
CrossRef Pubmed Google scholar
[74]
Zhang JP, Yan J, Xu J, Pang XH, Chen MS, Li L, Wu C, Li SP, Zheng L. Increased intratumoral IL-17-producing cells correlate with poor survival in hepatocellular carcinoma patients. J Hepatol2009; 50(5): 980-989
CrossRef Pubmed Google scholar
[75]
Laan M, Cui ZH, Hoshino H, Lötvall J, Sjöstrand M, Gruenert DC, Skoogh BE, Lindén A. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol1999; 162(4): 2347-2352
Pubmed
[76]
Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer2008; 8(8): 618-631
CrossRef Pubmed Google scholar
[77]
Kuang DM, Peng C, Zhao Q, Wu Y, Chen MS, Zheng L. Activated monocytes in peritumoral stroma of hepatocellular carcinoma promote expansion of memory T helper 17 cells. Hepatology2010; 51(1): 154-164
CrossRef Pubmed Google scholar
[78]
Zhao Q, Xiao X, Wu Y, Wei Y, Zhu LY, Zhou J, Kuang DM. Interleukin-17-educated monocytes suppress cytotoxic T-cell function through B7-H1 in hepatocellular carcinoma patients. Eur J Immunol2011; 41(8): 2314-2322
CrossRef Pubmed Google scholar
[79]
Oppmann B, Lesley R, Blom B, Timans JC, Xu Y, Hunte B, Vega F, Yu N, Wang J, Singh K, Zonin F, Vaisberg E, Churakova T, Liu M, Gorman D, Wagner J, Zurawski S, Liu Y, Abrams JS, Moore KW, Rennick D, de Waal-Malefyt R, Hannum C, Bazan JF, Kastelein RA. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity2000; 13(5): 715-725
CrossRef Pubmed Google scholar
[80]
Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, Sedgwick JD, Cua DJ. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med2003; 198(12): 1951-1957
CrossRef Pubmed Google scholar
[81]
Hue S, Ahern P, Buonocore S, Kullberg MC, Cua DJ, McKenzie BS, Powrie F, Maloy KJ. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med2006; 203(11): 2473-2483
CrossRef Pubmed Google scholar
[82]
Lo CH, Chang CM, Tang SW, Pan WY, Fang CC, Chen Y, Wu PY, Chen KY, Ma HI, Xiao X, Tao MH. Differential antitumor effect of interleukin-12 family cytokines on orthotopic hepatocellular carcinoma. J Gene Med2010; 12(5): 423-434
CrossRef Pubmed Google scholar
[83]
Hu P, Hu HD, Chen M, Peng ML, Tang L, Tang KF, Matsui M, Belladonna ML, Yoshimoto T, Zhang DZ, Xiang R, Ren H. Expression of interleukins-23 and 27 leads to successful gene therapy of hepatocellular carcinoma. Mol Immunol2009; 46(8-9): 1654-1662
CrossRef Pubmed Google scholar
[84]
Li J, Lau G, Chen L, Yuan YF, Huang J, Luk JM, Xie D, Guan XY. Interleukin 23 promotes hepatocellular carcinoma metastasis via NF-kappa B induced matrix metalloproteinase 9 expression. PLoS ONE2012; 7(9): e46264
CrossRef Pubmed Google scholar
[85]
Jiang R, Tan Z, Deng L, Chen Y, Xia Y, Gao Y, Wang X, Sun B. Interleukin-22 promotes human hepatocellular carcinoma by activation of STAT3. Hepatology2011; 54(3): 900-909
CrossRef Pubmed Google scholar
[86]
Lejeune D, Dumoutier L, Constantinescu S, Kruijer W, Schuringa JJ, Renauld JC. Interleukin-22 (IL-22) activates the JAK/STAT, ERK, JNK, and p38 MAP kinase pathways in a rat hepatoma cell line. Pathways that are shared with and distinct from IL-10. J Biol Chem2002; 277(37): 33676-33682
CrossRef Pubmed Google scholar
[87]
Zhang W, Chen Y, Wei H, Zheng C, Sun R, Zhang J, Tian Z. Antiapoptotic activity of autocrine interleukin-22 and therapeutic effects of interleukin-22-small interfering RNA on human lung cancer xenografts. Clin Cancer Res2008; 14(20): 6432-6439
CrossRef Pubmed Google scholar
[88]
Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Karow M, Flavell RA. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity2007; 27(4): 647-659
CrossRef Pubmed Google scholar
[89]
Park O, Wang H, Weng H, Feigenbaum L, Li H, Yin S, Ki SH, Yoo SH, Dooley S, Wang FS, Young HA, Gao B. In vivo consequences of liver-specific interleukin-22 expression in mice: Implications for human liver disease progression. Hepatology2011; 54(1): 252-261
CrossRef Pubmed Google scholar
[90]
Bertino G, Ardiri A, Malaguarnera M, Malaguarnera G, Bertino N, Calvagno GS. Hepatocellualar carcinoma serum markers. Semin Oncol2012; 39(4): 410-433
CrossRef Pubmed Google scholar
[91]
Hu J, Xu Y, Hao J, Wang S, Li C, Meng S. MiR-122 in hepatic function and liver diseases. Protein Cell2012; 3(5): 364-371
CrossRef Pubmed Google scholar
[92]
Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell2004; 116(2): 281-297
CrossRef Pubmed Google scholar
[93]
He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet2004; 5(7): 522-531
CrossRef Pubmed Google scholar
[94]
Sugatani T, Hruska KA. Down-regulation of miR-21 biogenesis by estrogen action contributes to osteoclastic apoptosis. J Cell Biochem2012; n/a
CrossRef Pubmed Google scholar
[95]
Mott JL. MicroRNAs involved in tumor suppressor and oncogene pathways: implications for hepatobiliary neoplasia. Hepatology2009; 50(2): 630-637
CrossRef Pubmed Google scholar
[96]
Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, Rebouissou S, Zucman-Rossi J. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology2008; 47(6): 1955-1963
CrossRef Pubmed Google scholar
[97]
Braconi C, Patel T. MicroRNA expression profiling: a molecular tool for defining the phenotype of hepatocellular tumors. Hepatology2008; 47(6): 1807-1809
CrossRef Pubmed Google scholar
[98]
Jiang J, Gusev Y, Aderca I, Mettler TA, Nagorney DM, Brackett DJ, Roberts LR, Schmittgen TD. Association of microRNA expression in hepatocellular carcinomas with hepatitis infection, cirrhosis, and patient survival. Clin Cancer Res2008; 14(2): 419-427
CrossRef Pubmed Google scholar
[99]
Kutay H, Bai S, Datta J, Motiwala T, Pogribny I, Frankel W, Jacob ST, Ghoshal K. Downregulation of miR-122 in the rodent and human hepatocellular carcinomas. J Cell Biochem2006; 99(3): 671-678
CrossRef Pubmed Google scholar
[100]
Murakami Y, Yasuda T, Saigo K, Urashima T, Toyoda H, Okanoue T, Shimotohno K. Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene2006; 25(17): 2537-2545
CrossRef Pubmed Google scholar
[101]
Li W, Xie L, He X, Li J, Tu K, Wei L, Wu J, Guo Y, Ma X, Zhang P, Pan Z, Hu X, Zhao Y, Xie H, Jiang G, Chen T, Wang J, Zheng S, Cheng J, Wan D, Yang S, Li Y, Gu J. Diagnostic and prognostic implications of microRNAs in human hepatocellular carcinoma. Int J Cancer2008; 123(7): 1616-1622
CrossRef Pubmed Google scholar
[102]
Wang Y, Lee AT, Ma JZ, Wang J, Ren J, Yang Y, Tantoso E, Li KB, Ooi LL, Tan P, Lee CG. Profiling microRNA expression in hepatocellular carcinoma reveals microRNA-224 up-regulation and apoptosis inhibitor-5 as a microRNA-224-specific target. J Biol Chem2008; 283(19): 13205-13215
CrossRef Pubmed Google scholar
[103]
Budhu A, Jia HL, Forgues M, Liu CG, Goldstein D, Lam A, Zanetti KA, Ye QH, Qin LX, Croce CM, Tang ZY, Wang XW. Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology2008; 47(3): 897-907
CrossRef Pubmed Google scholar
[104]
Gramantieri L, Ferracin M, Fornari F, Veronese A, Sabbioni S, Liu CG, Calin GA, Giovannini C, Ferrazzi E, Grazi GL, Croce CM, Bolondi L, Negrini M. Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res2007; 67(13): 6092-6099
CrossRef Pubmed Google scholar
[105]
Varnholt H, Drebber U, Schulze F, Wedemeyer I, Schirmacher P, Dienes HP, Odenthal M. MicroRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma. Hepatology2008; 47(4): 1223-1232
CrossRef Pubmed Google scholar
[106]
Wong QW, Lung RW, Law PT, Lai PB, Chan KY, To KF, Wong N. MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin1. Gastroenterology2008; 135(1): 257-269
CrossRef Pubmed Google scholar
[107]
Pineau P, Volinia S, McJunkin K, Marchio A, Battiston C, Terris B, Mazzaferro V, Lowe SW, Croce CM, Dejean A. miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci USA2010; 107(1): 264-269
CrossRef Pubmed Google scholar
[108]
Fan CG, Wang CM, Tian C, Wang Y, Li L, Sun WS, Li RF, Liu YG. miR-122 inhibits viral replication and cell proliferation in hepatitis B virus-related hepatocellular carcinoma and targets NDRG3. Oncol Rep2011; 26(5): 1281-1286
Pubmed
[109]
Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, David M. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature2007; 449(7164): 919-922
CrossRef Pubmed Google scholar
[110]
Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science2005; 309(5740): 1577-1581
CrossRef Pubmed Google scholar
[111]
Zhang X, Zhang E, Ma Z, Pei R, Jiang M, Schlaak JF, Roggendorf M, Lu M. Modulation of hepatitis B virus replication and hepatocyte differentiation by microRNA-1. Hepatology2011; 53(5): 1476-1485
CrossRef Pubmed Google scholar
[112]
Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH, Filipowicz W. Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat Med2009; 15(1): 31-33
CrossRef Pubmed Google scholar
[113]
van der Poorten D, George J. Disease-specific mechanisms of fibrosis: hepatitis C virus and nonalcoholic steatohepatitis. Clin Liver Dis2008; 12(4): 805-824, ix (ix.)
CrossRef Pubmed Google scholar
[114]
Whittaker R, Loy PA, Sisman E, Suyama E, Aza-Blanc P, Ingermanson RS, Price JH, McDonough PM. Identification of microRNAs that control lipid droplet formation and growth in hepatocytes via high-content screening. J Biomol Screen2010; 15(7): 798-805
CrossRef Pubmed Google scholar
[115]
Zheng L, Lv GC, Sheng J, Yang YD. Effect of miRNA-10b in regulating cellular steatosis level by targeting PPAR-alpha expression, a novel mechanism for the pathogenesis of NAFLD. J Gastroenterol Hepatol2010; 25(1): 156-163
CrossRef Pubmed Google scholar
[116]
Cheung O, Puri P, Eicken C, Contos MJ, Mirshahi F, Maher JW, Kellum JM, Min H, Luketic VA, Sanyal AJ. Nonalcoholic steatohepatitis is associated with altered hepatic microRNA expression. Hepatology2008; 48(6): 1810-1820
CrossRef Pubmed Google scholar
[117]
Song G, Sharma AD, Roll GR, Ng R, Lee AY, Blelloch RH, Frandsen NM, Willenbring H. MicroRNAs control hepatocyte proliferation during liver regeneration. Hepatology2010; 51(5): 1735-1743
CrossRef Pubmed Google scholar
[118]
Castro RE, Ferreira DM, Zhang X, Borralho PM, Sarver AL, Zeng Y, Steer CJ, Kren BT, Rodrigues CM. Identification of microRNAs during rat liver regeneration after partial hepatectomy and modulation by ursodeoxycholic acid. Am J Physiol Gastrointest Liver Physiol2010; 299(4): G887-G897
CrossRef Pubmed Google scholar
[119]
Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology2007; 133(2): 647-658
CrossRef Pubmed Google scholar
[120]
Marquez RT, Wendlandt E, Galle CS, Keck K, McCaffrey AP. MicroRNA-21 is upregulated during the proliferative phase of liver regeneration, targets Pellino-1, and inhibits NF-kappaB signaling. Am J Physiol Gastrointest Liver Physiol2010; 298(4): G535-G541
CrossRef Pubmed Google scholar
[121]
Lowes KN, Brennan BA, Yeoh GC, Olynyk JK. Oval cell numbers in human chronic liver diseases are directly related to disease severity. Am J Pathol1999; 154(2): 537-541
CrossRef Pubmed Google scholar
[122]
Libbrecht L, Desmet V, Van Damme B, Roskams T. Deep intralobular extension of human hepatic ‘progenitor cells’ correlates with parenchymal inflammation in chronic viral hepatitis: can ‘progenitor cells’ migrate? J Pathol2000; 192(3): 373-378
CrossRef Pubmed Google scholar
[123]
Viebahn CS, Yeoh GC. What fires prometheus? The link between inflammation and regeneration following chronic liver injury. Int J Biochem Cell Biol2008; 40(5): 855-873
CrossRef Pubmed Google scholar
[124]
Alison MR, Lovell MJ. Liver cancer: the role of stem cells. Cell Prolif2005; 38(6): 407-421
CrossRef Pubmed Google scholar
[125]
Theise ND, Yao JL, Harada K, Hytiroglou P, Portmann B, Thung SN, Tsui W, Ohta H, Nakanuma Y. Hepatic ‘stem cell’ malignancies in adults: four cases. Histopathology2003; 43(3): 263-271
CrossRef Pubmed Google scholar
[126]
Dumble ML, Croager EJ, Yeoh GC, Quail EA. Generation and characterization of p53 null transformed hepatic progenitor cells: oval cells give rise to hepatocellular carcinoma. Carcinogenesis2002; 23(3): 435-445
CrossRef Pubmed Google scholar
[127]
Korkaya H, Wicha MS. Selective targeting of cancer stem cells: a new concept in cancer therapeutics. BioDrugs2007; 21(5): 299-310
CrossRef Pubmed Google scholar
[128]
Wicha MS, Liu S, Dontu G. Cancer stem cells: an old idea—a paradigm shift. Cancer Res2006; 66(4): 1883-1890; discussion 1895-1896
Pubmed
[129]
Vermeulen L, De Sousa E Melo F, van der Heijden M, Cameron K, de Jong JH, Borovski T, Tuynman JB, Todaro M, Merz C, Rodermond H, Sprick MR, Kemper K, Richel DJ, Stassi G, Medema JP. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol2010; 12(5): 468-476
CrossRef Pubmed Google scholar
[130]
Polyak K, Haviv I, Campbell IG. Co-evolution of tumor cells and their microenvironment. Trends Genet2009; 25(1): 30-38
CrossRef Pubmed Google scholar
[131]
Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A, Gilbertson RJ. A perivascular niche for brain tumor stem cells. Cancer Cell2007; 11(1): 69-82
CrossRef Pubmed Google scholar
[132]
Stauffer JK, Scarzello AJ, Andersen JB, De Kluyver RL, Back TC, Weiss JM, Thorgeirsson SS, Wiltrout RH. Coactivation of AKT and β-catenin in mice rapidly induces formation of lipogenic liver tumors. Cancer Res2011; 71(7): 2718-2727
CrossRef Pubmed Google scholar
[133]
Schrader J, Gordon-Walker TT, Aucott RL, van Deemter M, Quaas A, Walsh S, Benten D, Forbes SJ, Wells RG, Iredale JP. Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology2011; 53(4): 1192-1205
CrossRef Pubmed Google scholar
[134]
Brunt EM, Blomenkamp K, Ahmed M, Ali F, Marcus N, Teckman J. Hepatic progenitor cell proliferation and liver injury in α-1-antitrypsin deficiency. J Pediatr Gastroenterol Nutr2010; 51(5): 626-630
CrossRef Pubmed Google scholar
[135]
Kitisin K, Shetty K, Mishra L, Johnson LB. Hepatocellular stem cells. Cancer Biomark2007; 3(4-5): 251-262
Pubmed
[136]
Yamashita T, Honda M, Nakamoto Y, Baba M, Nio K, Hara Y, Zeng SS, Hayashi T, Kondo M, Takatori H, Yamashita T, Mizukoshi E, Ikeda H, Zen Y, Takamura H, Wang XW, Kaneko S. Discrete nature of EpCAM(+) and CD90(+) cancer stem cells in human hepatocellular carcinoma. Hepatology2012; 57(4):1484-97
Pubmed
[137]
Jakubowski A, Ambrose C, Parr M, Lincecum JM, Wang MZ, Zheng TS, Browning B, Michaelson JS, Baetscher M, Wang B, Bissell DM, Burkly LC. TWEAK induces liver progenitor cell proliferation. J Clin Invest2005; 115(9): 2330-2340
CrossRef Pubmed Google scholar
[138]
Fausto N. Tweaking liver progenitor cells. Nat Med2005; 11(10): 1053-1054
CrossRef Pubmed Google scholar
[139]
Akhurst B, Matthews V, Husk K, Smyth MJ, Abraham LJ, Yeoh GC. Differential lymphotoxin-beta and interferon gamma signaling during mouse liver regeneration induced by chronic and acute injury. Hepatology2005; 41(2): 327-335
CrossRef Pubmed Google scholar
[140]
Uchio K, Graham M, Dean NM, Rosenbaum J, Desmoulière A. Down-regulation of connective tissue growth factor and type I collagen mRNA expression by connective tissue growth factor antisense oligonucleotide during experimental liver fibrosis. Wound Repair Regen2004; 12(1): 60-66
CrossRef Pubmed Google scholar
[141]
Nakamura K, Nonaka H, Saito H, Tanaka M, Miyajima A. Hepatocyte proliferation and tissue remodeling is impaired after liver injury in oncostatin M receptor knockout mice. Hepatology2004; 39(3): 635-644
CrossRef Pubmed Google scholar
[142]
Brooling JT, Campbell JS, Mitchell C, Yeoh GC, Fausto N. Differential regulation of rodent hepatocyte and oval cell proliferation by interferon gamma. Hepatology2005; 41(4): 906-915
CrossRef Pubmed Google scholar
[143]
Gangaraju VK, Lin H. MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol2009; 10(2): 116-125
CrossRef Pubmed Google scholar
[144]
Osborne JD, Flatow J, Holko M, Lin SM, Kibbe WA, Zhu LJ, Danila MI, Feng G, and Chisholm RL. Annotating the human genome with Disease Ontology. BMC Genomics.2009;10Suppl 1(S6.
[145]
Ji J, Yamashita T, Budhu A, Forgues M, Jia HL, Li C, Deng C, Wauthier E, Reid LM, Ye QH, Qin LX, Yang W, Wang HY, Tang ZY, Croce CM, Wang XW. Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology2009; 50(2): 472-480
CrossRef Pubmed Google scholar

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