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Published in: World Journal of Surgical Oncology 1/2013

Open Access 01-12-2013 | Research

Expression of glioma-associated oncogene 2 (Gli 2) is correlated with poor prognosis in patients with hepatocellular carcinoma undergoing hepatectomy

Authors: Dawei Zhang, Liangqi Cao, Yue Li, Haiwu Lu, Xuewei Yang, Ping Xue

Published in: World Journal of Surgical Oncology | Issue 1/2013

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Abstract

Background

Our previous studies showed that glioma-associated oncogene (Gli)2 plays an important role in the proliferation and apoptosis resistance of hepatocellular carcinoma (HCC) cells. The aim of this study was to explore the clinical significance of Gli2 expression in HCC.

Methods

Expression of Gli2 protein was detected in samples from 68 paired HCC samples, the corresponding paraneoplastic liver tissues, and 20 normal liver tissues using immunohistochemistry. Correlation of the immunohistochemistry results with clinicopathologic parameters, prognosis, and the expression of E-cadherin, N-cadherin, and vimentin were analyzed.

Results

Immunohistochemical staining showed high levels of Gli2 protein expression in HCC, compared with paraneoplastic and normal liver tissues (P < 0.05). This high expression level of Gli2 was significantly associated with tumor differentiation, encapsulation, vascular invasion, early recurrence, and intra-hepatic metastasis (P < 0.05). There was a significantly negative correlation between Gli2 and E-cadherin expression (r = −0.302, P < 0.05) and a significantly positive correlation between expression of Gli2 and expression of vimentin (r = −0.468, P < 0.05) and N-cadherin (r = −0.505, P < 0.05). Kaplan-Meier analysis showed that patients with overexpressed Gli2 had significantly shorter overall survival and disease-free survival times (P < 0.05). Multivariate analysis suggested that the level of Gli2 expression was an independent prognostic factor for HCC.

Conclusions

Expression of Gli2 is high in HCC tissue, and is associated with poor prognosis in patients with HCC after hepatectomy.
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Literature
1.
go back to reference Llovet JM, Burroughs A, Bruix J: Hepatocellular carcinoma. Lancet. 2003, 362: 1907-1917. 10.1016/S0140-6736(03)14964-1.CrossRefPubMed Llovet JM, Burroughs A, Bruix J: Hepatocellular carcinoma. Lancet. 2003, 362: 1907-1917. 10.1016/S0140-6736(03)14964-1.CrossRefPubMed
2.
3.
go back to reference Jemal A, Bray F, Center MM: Global cancer statistics. CA Cancer J Clin. 2011, 61: 69-90. 10.3322/caac.20107.CrossRefPubMed Jemal A, Bray F, Center MM: Global cancer statistics. CA Cancer J Clin. 2011, 61: 69-90. 10.3322/caac.20107.CrossRefPubMed
4.
go back to reference Parkin DM, Bray F, Ferlay J: Global cancer statistics, 2002. CA Cancer J Clin. 2005, 55: 74-108. 10.3322/canjclin.55.2.74.CrossRefPubMed Parkin DM, Bray F, Ferlay J: Global cancer statistics, 2002. CA Cancer J Clin. 2005, 55: 74-108. 10.3322/canjclin.55.2.74.CrossRefPubMed
5.
go back to reference Hubert C, Sempoux C, Rahier J: Prognostic risk factors of survival after resection of hepatocellular carcinoma. Hepatogastroenterology. 2007, 54: 1791-1797.PubMed Hubert C, Sempoux C, Rahier J: Prognostic risk factors of survival after resection of hepatocellular carcinoma. Hepatogastroenterology. 2007, 54: 1791-1797.PubMed
6.
go back to reference Sherman M: Recurrence of hepatocellular carcinoma. N Engl J Med. 2008, 359: 2045-2047. 10.1056/NEJMe0807581.CrossRefPubMed Sherman M: Recurrence of hepatocellular carcinoma. N Engl J Med. 2008, 359: 2045-2047. 10.1056/NEJMe0807581.CrossRefPubMed
7.
go back to reference Ingham PW, McMahon AP: Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 2001, 15: 3059-3087. 10.1101/gad.938601.CrossRefPubMed Ingham PW, McMahon AP: Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 2001, 15: 3059-3087. 10.1101/gad.938601.CrossRefPubMed
8.
go back to reference Ruizi Altaba A, Sanchez P, Dahmane N: Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat Rev Cancer. 2002, 2: 361-372. 10.1038/nrc796.CrossRef Ruizi Altaba A, Sanchez P, Dahmane N: Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat Rev Cancer. 2002, 2: 361-372. 10.1038/nrc796.CrossRef
9.
go back to reference Lum L, Beachy PA: The Hedgehog response network: sensors, switches, and routers. Science. 2004, 304: 1755-1759. 10.1126/science.1098020.CrossRefPubMed Lum L, Beachy PA: The Hedgehog response network: sensors, switches, and routers. Science. 2004, 304: 1755-1759. 10.1126/science.1098020.CrossRefPubMed
10.
go back to reference Berman DM, Karhadkar SS, Maitra A: Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature. 2003, 425: 846-851. 10.1038/nature01972.CrossRefPubMed Berman DM, Karhadkar SS, Maitra A: Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature. 2003, 425: 846-851. 10.1038/nature01972.CrossRefPubMed
11.
go back to reference Ji J, Kump E, Wernli M: Gene silencing of transcription factor Gli2 inhibits basal cell carcinomalike tumor growth in vivo. Int J Cancer. 2008, 122: 50-56. 10.1002/ijc.23023.CrossRefPubMed Ji J, Kump E, Wernli M: Gene silencing of transcription factor Gli2 inhibits basal cell carcinomalike tumor growth in vivo. Int J Cancer. 2008, 122: 50-56. 10.1002/ijc.23023.CrossRefPubMed
12.
go back to reference Kubo M, Nakamura M, Tasaki A: Hedgehog signaling pathway is a new therapeutic target for patients with breast cancer. Cancer Res. 2004, 64: 6071-6074. 10.1158/0008-5472.CAN-04-0416.CrossRefPubMed Kubo M, Nakamura M, Tasaki A: Hedgehog signaling pathway is a new therapeutic target for patients with breast cancer. Cancer Res. 2004, 64: 6071-6074. 10.1158/0008-5472.CAN-04-0416.CrossRefPubMed
13.
go back to reference Thayer SP, di Magliano MP, Heiser PW: Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature. 2003, 425: 851-856. 10.1038/nature02009.PubMedCentralCrossRefPubMed Thayer SP, di Magliano MP, Heiser PW: Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature. 2003, 425: 851-856. 10.1038/nature02009.PubMedCentralCrossRefPubMed
14.
go back to reference Thiyagarajan S, Bhatia N, Reagan-Shaw S: Role of GLI2 transcription factor in growth and tumorigenicity of prostate cells. Cancer Res. 2007, 67: 10642-10646. 10.1158/0008-5472.CAN-07-2015.PubMedCentralCrossRefPubMed Thiyagarajan S, Bhatia N, Reagan-Shaw S: Role of GLI2 transcription factor in growth and tumorigenicity of prostate cells. Cancer Res. 2007, 67: 10642-10646. 10.1158/0008-5472.CAN-07-2015.PubMedCentralCrossRefPubMed
15.
go back to reference Velcheti V, Govindan R: Hedgehog signaling pathway and lung cancer. J Thorac Oncol. 2007, 2: 7-10. 10.1097/JTO.0b013e31802c0276.CrossRefPubMed Velcheti V, Govindan R: Hedgehog signaling pathway and lung cancer. J Thorac Oncol. 2007, 2: 7-10. 10.1097/JTO.0b013e31802c0276.CrossRefPubMed
16.
go back to reference Von Hoff DD, LoRusso PM, Rudin CM: Inhibition of the hedgehog pathway in advanced basal-cell carcinoma. N Engl J Med. 2009, 361: 1164-1172. 10.1056/NEJMoa0905360.CrossRefPubMed Von Hoff DD, LoRusso PM, Rudin CM: Inhibition of the hedgehog pathway in advanced basal-cell carcinoma. N Engl J Med. 2009, 361: 1164-1172. 10.1056/NEJMoa0905360.CrossRefPubMed
17.
go back to reference Katoh Y, Katoh M: Hedgehog signaling, epithelial-to-mesenchymal transition and miRNA (review). Int J Mol Med. 2008, 22: 271-275.PubMed Katoh Y, Katoh M: Hedgehog signaling, epithelial-to-mesenchymal transition and miRNA (review). Int J Mol Med. 2008, 22: 271-275.PubMed
18.
go back to reference He HC, Chen JH, Chen XB: Expression of hedgehog pathway components is associated with bladder cancer progression and clinical outcome. Pathol Oncol Res. 2012, 18: 349-355. 10.1007/s12253-011-9451-2.CrossRefPubMed He HC, Chen JH, Chen XB: Expression of hedgehog pathway components is associated with bladder cancer progression and clinical outcome. Pathol Oncol Res. 2012, 18: 349-355. 10.1007/s12253-011-9451-2.CrossRefPubMed
19.
go back to reference Liao X, Siu MK, Au CW: Aberrant activation of hedgehog signaling pathway in ovarian cancers: effect on prognosis, cell invasion and differentiation. Carcinogenesis. 2009, 30: 131-140.CrossRefPubMed Liao X, Siu MK, Au CW: Aberrant activation of hedgehog signaling pathway in ovarian cancers: effect on prognosis, cell invasion and differentiation. Carcinogenesis. 2009, 30: 131-140.CrossRefPubMed
20.
go back to reference Mori Y, Okumura T, Tsunoda S: Gli-1 expression is associated with lymph node metastasis and tumor progression in esophageal squamous cell carcinoma. Oncology. 2006, 70: 378-389. 10.1159/000098111.CrossRefPubMed Mori Y, Okumura T, Tsunoda S: Gli-1 expression is associated with lymph node metastasis and tumor progression in esophageal squamous cell carcinoma. Oncology. 2006, 70: 378-389. 10.1159/000098111.CrossRefPubMed
21.
go back to reference ten Haaf A, Bektas N, von Serenyi S: Expression of the glioma-associated oncogene homolog (GLI) 1 in human breast cancer is associated with unfavourable overall survival. BMC Cancer. 2009, 9: 298-310. 10.1186/1471-2407-9-298.PubMedCentralCrossRefPubMed ten Haaf A, Bektas N, von Serenyi S: Expression of the glioma-associated oncogene homolog (GLI) 1 in human breast cancer is associated with unfavourable overall survival. BMC Cancer. 2009, 9: 298-310. 10.1186/1471-2407-9-298.PubMedCentralCrossRefPubMed
22.
go back to reference Xu M, Li X, Liu T: Prognostic value of hedgehog signaling pathway in patients with colon cancer. Med Oncol. 2012, 29: 1010-6. 10.1007/s12032-011-9899-7.CrossRefPubMed Xu M, Li X, Liu T: Prognostic value of hedgehog signaling pathway in patients with colon cancer. Med Oncol. 2012, 29: 1010-6. 10.1007/s12032-011-9899-7.CrossRefPubMed
23.
go back to reference Yan M, Wang L, Zuo H: HH/GLI signalling as a new therapeutic target for patients with oral squamous cell carcinoma. Oral Oncol. 2011, 47: 504-509. 10.1016/j.oraloncology.2011.03.027.CrossRefPubMed Yan M, Wang L, Zuo H: HH/GLI signalling as a new therapeutic target for patients with oral squamous cell carcinoma. Oral Oncol. 2011, 47: 504-509. 10.1016/j.oraloncology.2011.03.027.CrossRefPubMed
24.
go back to reference Ikram MS, Neill GW, Regl G: GLI2 is expressed in normal human epidermis and BCC and induces GLI1 expression by binding to its promoter. J Invest Dermatol. 2004, 122: 1503-1509. 10.1111/j.0022-202X.2004.22612.x.CrossRefPubMed Ikram MS, Neill GW, Regl G: GLI2 is expressed in normal human epidermis and BCC and induces GLI1 expression by binding to its promoter. J Invest Dermatol. 2004, 122: 1503-1509. 10.1111/j.0022-202X.2004.22612.x.CrossRefPubMed
25.
go back to reference Cheng WT, Xu K, Tian DY: Role of Hedgehog signaling pathway in proliferation and invasiveness of hepatocellular carcinoma cells. Int J Oncol. 2009, 34: 829-836.PubMed Cheng WT, Xu K, Tian DY: Role of Hedgehog signaling pathway in proliferation and invasiveness of hepatocellular carcinoma cells. Int J Oncol. 2009, 34: 829-836.PubMed
26.
go back to reference Kim Y, Yoon JW, Xiao X: Selective down-regulation of glioma-associated oncogene 2 inhibits the proliferation of hepatocellular carcinoma cells. Cancer Res. 2007, 67: 3583-3593. 10.1158/0008-5472.CAN-06-3040.CrossRefPubMed Kim Y, Yoon JW, Xiao X: Selective down-regulation of glioma-associated oncogene 2 inhibits the proliferation of hepatocellular carcinoma cells. Cancer Res. 2007, 67: 3583-3593. 10.1158/0008-5472.CAN-06-3040.CrossRefPubMed
27.
go back to reference Patil MA, Zhang J, Ho C: Hedgehog signaling in human hepatocellular carcinoma. Cancer Biol Ther. 2006, 5: 111-117. 10.4161/cbt.5.1.2379.CrossRefPubMed Patil MA, Zhang J, Ho C: Hedgehog signaling in human hepatocellular carcinoma. Cancer Biol Ther. 2006, 5: 111-117. 10.4161/cbt.5.1.2379.CrossRefPubMed
28.
go back to reference Sicklick JK, Li YX, Jayaraman A: Dysregulation of the Hedgehog pathway in human hepatocarcinogenesis. Carcinogenesis. 2006, 27: 748-757.CrossRefPubMed Sicklick JK, Li YX, Jayaraman A: Dysregulation of the Hedgehog pathway in human hepatocarcinogenesis. Carcinogenesis. 2006, 27: 748-757.CrossRefPubMed
29.
go back to reference Zhang D, Liu J, Wang Y: ShRNA-mediated silencing of Gli2 gene inhibits proliferation and sensitizes human hepatocellular carcinoma cells towards TRAIL-induced apoptosis. J Cell Biochem. 2011, 112: 3140-3150. 10.1002/jcb.23240.CrossRefPubMed Zhang D, Liu J, Wang Y: ShRNA-mediated silencing of Gli2 gene inhibits proliferation and sensitizes human hepatocellular carcinoma cells towards TRAIL-induced apoptosis. J Cell Biochem. 2011, 112: 3140-3150. 10.1002/jcb.23240.CrossRefPubMed
30.
go back to reference Dai DL, Martinka M, Li G: Prognostic significance of activated Akt expression in melanoma: a clinicopathologic study of 292 cases. J Clin Oncol. 2005, 23: 1473-1482. 10.1200/JCO.2005.07.168.CrossRefPubMed Dai DL, Martinka M, Li G: Prognostic significance of activated Akt expression in melanoma: a clinicopathologic study of 292 cases. J Clin Oncol. 2005, 23: 1473-1482. 10.1200/JCO.2005.07.168.CrossRefPubMed
31.
go back to reference Wang Y, Dai DL, Martinka M: Prognostic significance of nuclear ING3 expression in human cutaneous melanoma. Clin Cancer Res. 2007, 13: 4111-4116. 10.1158/1078-0432.CCR-07-0408.CrossRefPubMed Wang Y, Dai DL, Martinka M: Prognostic significance of nuclear ING3 expression in human cutaneous melanoma. Clin Cancer Res. 2007, 13: 4111-4116. 10.1158/1078-0432.CCR-07-0408.CrossRefPubMed
32.
go back to reference Eichberger T, Sander V, Schnidar H: Overlapping and distinct transcriptional regulator properties of the GLI1 and GLI2 oncogenes. Genomics. 2006, 87: 616-632. 10.1016/j.ygeno.2005.12.003.CrossRefPubMed Eichberger T, Sander V, Schnidar H: Overlapping and distinct transcriptional regulator properties of the GLI1 and GLI2 oncogenes. Genomics. 2006, 87: 616-632. 10.1016/j.ygeno.2005.12.003.CrossRefPubMed
33.
go back to reference Grachtchouk V, Grachtchouk M, Lowe L: The magnitude of hedgehog signaling activity defines skin tumor phenotype. EMBO J. 2003, 22: 2741-2751. 10.1093/emboj/cdg271.PubMedCentralCrossRefPubMed Grachtchouk V, Grachtchouk M, Lowe L: The magnitude of hedgehog signaling activity defines skin tumor phenotype. EMBO J. 2003, 22: 2741-2751. 10.1093/emboj/cdg271.PubMedCentralCrossRefPubMed
34.
go back to reference Kump E, Ji J, Wernli M: Gli2 upregulates cFlip and renders basal cell carcinoma cells resistant to death ligand-mediated apoptosis. Oncogene. 2008, 27: 3856-3864. 10.1038/onc.2008.5.CrossRefPubMed Kump E, Ji J, Wernli M: Gli2 upregulates cFlip and renders basal cell carcinoma cells resistant to death ligand-mediated apoptosis. Oncogene. 2008, 27: 3856-3864. 10.1038/onc.2008.5.CrossRefPubMed
35.
go back to reference Regl G, Kasper M, Schnidar H: Activation of the BCL2 promoter in response to Hedgehog/GLI signal transduction is predominantly mediated by GLI2. Cancer Res. 2004, 64: 7724-7731. 10.1158/0008-5472.CAN-04-1085.CrossRefPubMed Regl G, Kasper M, Schnidar H: Activation of the BCL2 promoter in response to Hedgehog/GLI signal transduction is predominantly mediated by GLI2. Cancer Res. 2004, 64: 7724-7731. 10.1158/0008-5472.CAN-04-1085.CrossRefPubMed
36.
go back to reference Fulda S, Meyer E, Debatin KM: Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression. Oncogene. 2002, 21: 2283-2294. 10.1038/sj.onc.1205258.CrossRefPubMed Fulda S, Meyer E, Debatin KM: Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression. Oncogene. 2002, 21: 2283-2294. 10.1038/sj.onc.1205258.CrossRefPubMed
37.
go back to reference Jin CY, Park C, Moon SK: Genistein sensitizes human hepatocellular carcinoma cells to TRAIL-mediated apoptosis by enhancing Bid cleavage. Anticancer Drugs. 2009, 20: 713-722. 10.1097/CAD.0b013e32832e8998.CrossRefPubMed Jin CY, Park C, Moon SK: Genistein sensitizes human hepatocellular carcinoma cells to TRAIL-mediated apoptosis by enhancing Bid cleavage. Anticancer Drugs. 2009, 20: 713-722. 10.1097/CAD.0b013e32832e8998.CrossRefPubMed
38.
go back to reference Okano H, Shiraki K, Inoue H: Cellular FLICE/caspase-8-inhibitory protein as a principal regulator of cell death and survival in human hepatocellular carcinoma. Lab Invest. 2003, 83: 1033-1043. 10.1097/01.LAB.0000079328.76631.28.CrossRefPubMed Okano H, Shiraki K, Inoue H: Cellular FLICE/caspase-8-inhibitory protein as a principal regulator of cell death and survival in human hepatocellular carcinoma. Lab Invest. 2003, 83: 1033-1043. 10.1097/01.LAB.0000079328.76631.28.CrossRefPubMed
39.
go back to reference Lin M, Guo LM, Liu H: Nuclear accumulation of glioma-associated oncogene 2 protein and enhanced expression of forkhead-box transcription factor M1 protein in human hepatocellular carcinoma. Histol Histopathol. 2010, 25: 1269-1275.PubMed Lin M, Guo LM, Liu H: Nuclear accumulation of glioma-associated oncogene 2 protein and enhanced expression of forkhead-box transcription factor M1 protein in human hepatocellular carcinoma. Histol Histopathol. 2010, 25: 1269-1275.PubMed
40.
go back to reference Blanco MJ, Moreno-Bueno G, Sarrio D: Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene. 2002, 21: 3241-3246. 10.1038/sj.onc.1205416.CrossRefPubMed Blanco MJ, Moreno-Bueno G, Sarrio D: Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene. 2002, 21: 3241-3246. 10.1038/sj.onc.1205416.CrossRefPubMed
41.
go back to reference Ramis-Conde I, Drasdo D, Anderson AR: Modeling the influence of the E-cadherin-beta-catenin pathway in cancer cell invasion: a multiscale approach. Biophys J. 2008, 95: 155-165. 10.1529/biophysj.107.114678.PubMedCentralCrossRefPubMed Ramis-Conde I, Drasdo D, Anderson AR: Modeling the influence of the E-cadherin-beta-catenin pathway in cancer cell invasion: a multiscale approach. Biophys J. 2008, 95: 155-165. 10.1529/biophysj.107.114678.PubMedCentralCrossRefPubMed
42.
go back to reference Zheng X, Yao Y, Xu Q: Evaluation of glioma-associated oncogene 1 expression and its correlation with the expression of sonic hedgehog, E-cadherin and S100a4 in human hepatocellular carcinoma. Mol Med Report. 2010, 3: 965-970. Zheng X, Yao Y, Xu Q: Evaluation of glioma-associated oncogene 1 expression and its correlation with the expression of sonic hedgehog, E-cadherin and S100a4 in human hepatocellular carcinoma. Mol Med Report. 2010, 3: 965-970.
43.
go back to reference Barrallo-Gimeno A, Nieto MA: The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development. 2005, 132: 3151-3161. 10.1242/dev.01907.CrossRefPubMed Barrallo-Gimeno A, Nieto MA: The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development. 2005, 132: 3151-3161. 10.1242/dev.01907.CrossRefPubMed
44.
go back to reference Castro Alves C, Rosivatz E, Schott C: Slug is overexpressed in gastric carcinomas and may act synergistically with SIP1 and Snail in the down-regulat ion of E-cadherin. J Pathol. 2007, 211: 507-515. 10.1002/path.2138.CrossRefPubMed Castro Alves C, Rosivatz E, Schott C: Slug is overexpressed in gastric carcinomas and may act synergistically with SIP1 and Snail in the down-regulat ion of E-cadherin. J Pathol. 2007, 211: 507-515. 10.1002/path.2138.CrossRefPubMed
45.
go back to reference Katoh M: Epithelial-mesenchymal transition in gastric cancer (Review). Int J Oncol. 2005, 27: 1677-1683.PubMed Katoh M: Epithelial-mesenchymal transition in gastric cancer (Review). Int J Oncol. 2005, 27: 1677-1683.PubMed
46.
go back to reference Lee JM, Dedhar S, Kalluri R: The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol. 2006, 172: 973-981. 10.1083/jcb.200601018.PubMedCentralCrossRefPubMed Lee JM, Dedhar S, Kalluri R: The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol. 2006, 172: 973-981. 10.1083/jcb.200601018.PubMedCentralCrossRefPubMed
47.
go back to reference Rosivatz E, Becker I, Specht K: Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am J Pathol. 2002, 161: 1881-1891. 10.1016/S0002-9440(10)64464-1.PubMedCentralCrossRefPubMed Rosivatz E, Becker I, Specht K: Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am J Pathol. 2002, 161: 1881-1891. 10.1016/S0002-9440(10)64464-1.PubMedCentralCrossRefPubMed
48.
go back to reference Zheng X, Rumie Vittar NB, Gai X: The transcription factor GLI1 mediates TGFβ1 driven EMT in hepatocellular carcinoma via a SNAI1-dependent mechanism. PLoS One. 2012, 7: e49581-10.1371/journal.pone.0049581.PubMedCentralCrossRefPubMed Zheng X, Rumie Vittar NB, Gai X: The transcription factor GLI1 mediates TGFβ1 driven EMT in hepatocellular carcinoma via a SNAI1-dependent mechanism. PLoS One. 2012, 7: e49581-10.1371/journal.pone.0049581.PubMedCentralCrossRefPubMed
49.
go back to reference Thiery JP, Acloque H, Huang RY: Epithelial-mesenchymal transitions in development and disease. Cell. 2009, 139: 871-890. 10.1016/j.cell.2009.11.007.CrossRefPubMed Thiery JP, Acloque H, Huang RY: Epithelial-mesenchymal transitions in development and disease. Cell. 2009, 139: 871-890. 10.1016/j.cell.2009.11.007.CrossRefPubMed
50.
Metadata
Title
Expression of glioma-associated oncogene 2 (Gli 2) is correlated with poor prognosis in patients with hepatocellular carcinoma undergoing hepatectomy
Authors
Dawei Zhang
Liangqi Cao
Yue Li
Haiwu Lu
Xuewei Yang
Ping Xue
Publication date
01-12-2013
Publisher
BioMed Central
Published in
World Journal of Surgical Oncology / Issue 1/2013
Electronic ISSN: 1477-7819
DOI
https://doi.org/10.1186/1477-7819-11-25

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