Skip to main content
Top
Published in: Diagnostic Pathology 1/2014

Open Access 01-12-2014 | Research

Combined aberrant expression of N-Myc downstream-regulated gene 2 and CD24 is associated with disease-free survival and overall survival in patients with hepatocellular carcinoma

Authors: Bing Li, Qing Shao, Dong Ji, Fan Li, Xiaodong Guo, Guofeng Chen

Published in: Diagnostic Pathology | Issue 1/2014

Login to get access

Abstract

Background

N-Myc downstream-regulated gene 2 (NDRG2), as a tumor suppressor, has been demonstrated to inhibit tumor invasion and migration of hepatocellular carcinoma (HCC) by reducing the expression of CD24, which has been identified as a prognostic factor for HCC patients. However, the clinical significance of combined NDRG2 and CD24 expression in HCC remains unclear. Thus, the aim of the current study was to investigate the relationship of NDRG2 and CD24 expression with clinicopathological parameters and patients' survival.

Methods

Immunohistochemistry was performed to detect the expression and subcellular localizations of NDRG2 and CD24 proteins in 130 pairs of HCC and adjacent nonneoplastic liver tissues.

Results

NDRG2 protein was strongly expressed in the cytoplasm and plasma membrane of hepatocytes in adjacent nonneoplastic liver tissues, whereas its immunostaining was weak or negative in HCC tissues. In contrast, CD24 protein exhibited the cytoplasm immunostaining in tumor cells of HCC tissues but showed negative expression in adjacent nonneoplastic liver tissues. The statistical analysis also showed that the expression levels of NDRG2 and CD24 proteins in HCC tissues were respectively lower and higher than those in adjacent nonneoplastic liver tissues significantly (both P < 0.001). In addition, there was an inverse correlation between NDRG2 expression and CD24 expression in HCC tissues (P = 0.02). Moreover, combined NDRG2 downregulation and CD24 upregulation (NDRG2-low/CD24-high) more frequently occurred in HCC tissues with high serum AFP (P = 0.03), advanced tumor stage (P = 0.001) and high tumor grade (P = 0.02). Furthermore, HCC patients with NDRG2-low/CD24-high expression showed shortest 5-year disease-free survival and 5-year overall survival (both P < 0.001) of four groups (NDRG2-low/CD24-high, NDRG2-low/CD24-low, NDRG2-high/CD24-high, NDRG2-high/CD24-low). Of note, the multivariate survival analysis showed that the combined aberrant expression of NDRG2 and CD24 proteins was an independent prognostic factor for both 5-year disease-free survival and 5-year overall survival (both P = 0.01) in HCC.

Conclusions

These findings suggest that the downregulation of NDRG2 combined with the upregulation of CD24 may play a synergistic role in the occurrence and progression of HCC. A combined detection of NDRG2/CD24 expression may benefit us in determining the prognosis in patients with HCC.

Virtual Slides

Appendix
Available only for authorised users
Literature
1.
go back to reference Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D: Global cancer statistics. CA Cancer J Clin. 2011, 61: 69-90. 10.3322/caac.20107.PubMedCrossRef Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D: Global cancer statistics. CA Cancer J Clin. 2011, 61: 69-90. 10.3322/caac.20107.PubMedCrossRef
2.
go back to reference Kiyosawa K, Umemura T, Ichijo T, Matsumoto A, Yoshizawa K, Gad A, Tanaka E: Hepatocellular carcinoma: recent trends in Japan. Gastroenterology. 2004, 127: S17-S26. 10.1053/j.gastro.2004.09.012.PubMedCrossRef Kiyosawa K, Umemura T, Ichijo T, Matsumoto A, Yoshizawa K, Gad A, Tanaka E: Hepatocellular carcinoma: recent trends in Japan. Gastroenterology. 2004, 127: S17-S26. 10.1053/j.gastro.2004.09.012.PubMedCrossRef
3.
go back to reference Nguyen VT, Law MG, Dore GJ: Hepatitis B-related hepatocellular carcinoma: epidemiological characteristics and disease burden. J Viral Hepat. 2009, 16: 453-463. 10.1111/j.1365-2893.2009.01117.x.PubMedCrossRef Nguyen VT, Law MG, Dore GJ: Hepatitis B-related hepatocellular carcinoma: epidemiological characteristics and disease burden. J Viral Hepat. 2009, 16: 453-463. 10.1111/j.1365-2893.2009.01117.x.PubMedCrossRef
4.
go back to reference Dhanasekaran R, Limaye A, Cabrera R: Hepatocellular carcinoma: current trends in worldwide epidemiology, risk factors, diagnosis, and therapeutics. Hepat Med. 2012, 4: 19-37.PubMedPubMedCentral Dhanasekaran R, Limaye A, Cabrera R: Hepatocellular carcinoma: current trends in worldwide epidemiology, risk factors, diagnosis, and therapeutics. Hepat Med. 2012, 4: 19-37.PubMedPubMedCentral
5.
go back to reference Mordalska A, Latek J, Ferenc T, Pomorski L, Gałecka E, Zygmunt A, Lewiński A: Evaluation of NDRG2 gene expression in primary papillary thyroid carcinoma and in metastases of this neoplasm to regional lymph nodes. Thyroid Res. 2010, 3: 6-10.1186/1756-6614-3-6.PubMedPubMedCentralCrossRef Mordalska A, Latek J, Ferenc T, Pomorski L, Gałecka E, Zygmunt A, Lewiński A: Evaluation of NDRG2 gene expression in primary papillary thyroid carcinoma and in metastases of this neoplasm to regional lymph nodes. Thyroid Res. 2010, 3: 6-10.1186/1756-6614-3-6.PubMedPubMedCentralCrossRef
6.
go back to reference Kim MJ, Lim J, Yang Y, Lee MS, Lim JS: N-myc downstream-regulated gene 2 (NDRG2) suppresses the epithelial-mesenchymal transition (EMT) in breast cancer cells via STAT3/Snail signaling. Cancer Lett. 2014, 354: 33-42. 10.1016/j.canlet.2014.06.023.PubMedCrossRef Kim MJ, Lim J, Yang Y, Lee MS, Lim JS: N-myc downstream-regulated gene 2 (NDRG2) suppresses the epithelial-mesenchymal transition (EMT) in breast cancer cells via STAT3/Snail signaling. Cancer Lett. 2014, 354: 33-42. 10.1016/j.canlet.2014.06.023.PubMedCrossRef
7.
go back to reference Liu J, Zhang J, Wang X, Li Y, Chen Y, Li K, Zhang J, Yao L, Guo G: HIF-1 and NDRG2 contribute to hypoxia-induced radioresistance of cervical cancer Hela cells. Exp Cell Res. 2010, 316: 1985-1993. 10.1016/j.yexcr.2010.02.028.PubMedCrossRef Liu J, Zhang J, Wang X, Li Y, Chen Y, Li K, Zhang J, Yao L, Guo G: HIF-1 and NDRG2 contribute to hypoxia-induced radioresistance of cervical cancer Hela cells. Exp Cell Res. 2010, 316: 1985-1993. 10.1016/j.yexcr.2010.02.028.PubMedCrossRef
8.
go back to reference Deng Y, Yao L, Chau L, Ng SS, Peng Y, Liu X, Au WS, Wang J, Li F, Ji S, Han H, Nie X, Li Q, Kung HF, Leung SY, Lin MC: N-Myc downstream-regulated gene 2 (NDRG2) inhibits glioblastoma cell proliferation. Int J Cancer. 2003, 106: 342-347. 10.1002/ijc.11228.PubMedCrossRef Deng Y, Yao L, Chau L, Ng SS, Peng Y, Liu X, Au WS, Wang J, Li F, Ji S, Han H, Nie X, Li Q, Kung HF, Leung SY, Lin MC: N-Myc downstream-regulated gene 2 (NDRG2) inhibits glioblastoma cell proliferation. Int J Cancer. 2003, 106: 342-347. 10.1002/ijc.11228.PubMedCrossRef
9.
go back to reference Zhao H, Zhang J, Lu J, He X, Chen C, Li X, Gong L, Bao G, Fu Q, Chen S, Lin W, Shi H, Ma J, Liu X, Ma Q, Yao L: Reduced expression of N-Myc downstream-regulated gene 2 in human thyroid cancer. BMC Cancer. 2008, 8: 303-10.1186/1471-2407-8-303.PubMedPubMedCentralCrossRef Zhao H, Zhang J, Lu J, He X, Chen C, Li X, Gong L, Bao G, Fu Q, Chen S, Lin W, Shi H, Ma J, Liu X, Ma Q, Yao L: Reduced expression of N-Myc downstream-regulated gene 2 in human thyroid cancer. BMC Cancer. 2008, 8: 303-10.1186/1471-2407-8-303.PubMedPubMedCentralCrossRef
10.
go back to reference Liang ZL, Kang K, Yoon S, Huang SM, Lim JS, Kim JM, Lim JS, Lee HJ: NDRG2 is involved in the oncogenic properties of renal cell carcinoma and its loss is a novel independent poor prognostic factor after nephrectomy. Ann Surg Oncol. 2012, 19: 2763-2772. 10.1245/s10434-011-2204-3.PubMedCrossRef Liang ZL, Kang K, Yoon S, Huang SM, Lim JS, Kim JM, Lim JS, Lee HJ: NDRG2 is involved in the oncogenic properties of renal cell carcinoma and its loss is a novel independent poor prognostic factor after nephrectomy. Ann Surg Oncol. 2012, 19: 2763-2772. 10.1245/s10434-011-2204-3.PubMedCrossRef
11.
go back to reference Lorentzen A, Lewinsky RH, Bornholdt J, Vogel LK, Mitchelmore C: Expression profile of the N-myc Downstream Regulated Gene 2 (NDRG2) in human cancers with focus on breast cancer. BMC Cancer. 2011, 11: 14-10.1186/1471-2407-11-14.PubMedPubMedCentralCrossRef Lorentzen A, Lewinsky RH, Bornholdt J, Vogel LK, Mitchelmore C: Expression profile of the N-myc Downstream Regulated Gene 2 (NDRG2) in human cancers with focus on breast cancer. BMC Cancer. 2011, 11: 14-10.1186/1471-2407-11-14.PubMedPubMedCentralCrossRef
12.
go back to reference Lee DC, Kang YK, Kim WH, Jang YJ, Kim DJ, Park IY, Sohn BH, Sohn HA, Lee HG, Lim JS, Kim JW, Song EY, Kim DM, Lee MN, Oh GT, Kim SJ, Park KC, Yoo HS, Choi JY, Yeom YI: Functional and clinical evidence for NDRG2 as a candidate suppressor of liver cancer metastasis. Cancer Res. 2008, 68: 4210-4220. 10.1158/0008-5472.CAN-07-5040.PubMedCrossRef Lee DC, Kang YK, Kim WH, Jang YJ, Kim DJ, Park IY, Sohn BH, Sohn HA, Lee HG, Lim JS, Kim JW, Song EY, Kim DM, Lee MN, Oh GT, Kim SJ, Park KC, Yoo HS, Choi JY, Yeom YI: Functional and clinical evidence for NDRG2 as a candidate suppressor of liver cancer metastasis. Cancer Res. 2008, 68: 4210-4220. 10.1158/0008-5472.CAN-07-5040.PubMedCrossRef
13.
go back to reference Feng L, Xie Y, Zhang H, Wu Y: Down-regulation of NDRG2 gene expression in human colorectal cancer involves promoter methylation and microRNA-650. Biochem Biophys Res Commun. 2011, 406: 534-538. 10.1016/j.bbrc.2011.02.081.PubMedCrossRef Feng L, Xie Y, Zhang H, Wu Y: Down-regulation of NDRG2 gene expression in human colorectal cancer involves promoter methylation and microRNA-650. Biochem Biophys Res Commun. 2011, 406: 534-538. 10.1016/j.bbrc.2011.02.081.PubMedCrossRef
14.
go back to reference Yu C, Wu G, Dang N, Zhang W, Zhang R, Yan W, Zhao Y, Gao L, Wang Y, Beckwith N, Yuan J, Yao L: Inhibition of N-myc downstream-regulated gene 2 in prostatic carcinoma. Cancer Biol Ther. 2011, 12: 304-313. 10.4161/cbt.12.4.16382.PubMedCrossRef Yu C, Wu G, Dang N, Zhang W, Zhang R, Yan W, Zhao Y, Gao L, Wang Y, Beckwith N, Yuan J, Yao L: Inhibition of N-myc downstream-regulated gene 2 in prostatic carcinoma. Cancer Biol Ther. 2011, 12: 304-313. 10.4161/cbt.12.4.16382.PubMedCrossRef
15.
go back to reference Yao L, Zhang J, Liu X: NDRG2: a Myc-repressed gene involved in cancer and cell stress. Acta Biochim Biophys Sin (Shanghai). 2008, 40: 625-635. 10.1111/j.1745-7270.2008.00434.x.CrossRef Yao L, Zhang J, Liu X: NDRG2: a Myc-repressed gene involved in cancer and cell stress. Acta Biochim Biophys Sin (Shanghai). 2008, 40: 625-635. 10.1111/j.1745-7270.2008.00434.x.CrossRef
16.
go back to reference Liu N, Wang L, Liu X, Yang Q, Zhang J, Zhang W, Wu Y, Shen L, Zhang Y, Yang A, Han H, Zhang J, Yao L: Promoter methylation, mutation, and genomic deletion are involved in the decreased NDRG2 expression levels in several cancer cell lines. Biochem Biophys Res Commun. 2007, 358: 164-169. 10.1016/j.bbrc.2007.04.089.PubMedCrossRef Liu N, Wang L, Liu X, Yang Q, Zhang J, Zhang W, Wu Y, Shen L, Zhang Y, Yang A, Han H, Zhang J, Yao L: Promoter methylation, mutation, and genomic deletion are involved in the decreased NDRG2 expression levels in several cancer cell lines. Biochem Biophys Res Commun. 2007, 358: 164-169. 10.1016/j.bbrc.2007.04.089.PubMedCrossRef
17.
go back to reference Choi SC, Yoon SR, Park YP, Song EY, Kim JW, Kim WH, Yang Y, Lim JS, Lee HG: Expression of NDRG2 is related to tumor progression and survival of gastric cancer patients through Fas-mediated cell death. Exp Mol Med. 2007, 39: 705-714. 10.1038/emm.2007.77.PubMedCrossRef Choi SC, Yoon SR, Park YP, Song EY, Kim JW, Kim WH, Yang Y, Lim JS, Lee HG: Expression of NDRG2 is related to tumor progression and survival of gastric cancer patients through Fas-mediated cell death. Exp Mol Med. 2007, 39: 705-714. 10.1038/emm.2007.77.PubMedCrossRef
18.
go back to reference Zheng J, Li Y, Yang J, Liu Q, Shi M, Zhang R, Shi H, Ren Q, Ma J, Guo H, Tao Y, Xue Y, Jiang N, Yao L, Liu W: NDRG2 inhibits hepatocellular carcinoma adhesion, migration and invasion by regulating CD24 expression. BMC Cancer. 2011, 251: 1-9. Zheng J, Li Y, Yang J, Liu Q, Shi M, Zhang R, Shi H, Ren Q, Ma J, Guo H, Tao Y, Xue Y, Jiang N, Yao L, Liu W: NDRG2 inhibits hepatocellular carcinoma adhesion, migration and invasion by regulating CD24 expression. BMC Cancer. 2011, 251: 1-9.
19.
go back to reference Kristiansen G, Sammar M, Altevogt P: Tumour biological aspects of CD24, a mucin-like adhesion molecule. J Mol Histol. 2004, 35: 255-262. 10.1023/B:HIJO.0000032357.16261.c5.PubMedCrossRef Kristiansen G, Sammar M, Altevogt P: Tumour biological aspects of CD24, a mucin-like adhesion molecule. J Mol Histol. 2004, 35: 255-262. 10.1023/B:HIJO.0000032357.16261.c5.PubMedCrossRef
20.
go back to reference Cufí S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Vellon L, Menendez JA: Autophagy positively regulates the CD44(+) CD24(-/low) breast cancer stem-like phenotype. Cell Cycle. 2011, 10: 3871-3885. 10.4161/cc.10.22.17976.PubMedCrossRef Cufí S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Vellon L, Menendez JA: Autophagy positively regulates the CD44(+) CD24(-/low) breast cancer stem-like phenotype. Cell Cycle. 2011, 10: 3871-3885. 10.4161/cc.10.22.17976.PubMedCrossRef
21.
go back to reference Aigner S, Sthoeger ZM, Fogel M, Weber E, Zarn J, Ruppert M, Zeller Y, Vestweber D, Stahel R, Sammar M, Altevogt P: CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood. 1997, 89: 3385-3395.PubMed Aigner S, Sthoeger ZM, Fogel M, Weber E, Zarn J, Ruppert M, Zeller Y, Vestweber D, Stahel R, Sammar M, Altevogt P: CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood. 1997, 89: 3385-3395.PubMed
22.
go back to reference Karran L, Jones M, Morley G, Van Noorden S, Smith P, Lampert I, Griffin BE: Expression of a B-cell marker, CD24, on nasopharyngeal carcinoma cells. Int J Cancer. 1995, 60: 562-566. 10.1002/ijc.2910600422.PubMedCrossRef Karran L, Jones M, Morley G, Van Noorden S, Smith P, Lampert I, Griffin BE: Expression of a B-cell marker, CD24, on nasopharyngeal carcinoma cells. Int J Cancer. 1995, 60: 562-566. 10.1002/ijc.2910600422.PubMedCrossRef
23.
go back to reference Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH, Goulet R, Badve S, Nakshatri H: CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res. 2006, 8: R59-10.1186/bcr1610.PubMedPubMedCentralCrossRef Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH, Goulet R, Badve S, Nakshatri H: CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res. 2006, 8: R59-10.1186/bcr1610.PubMedPubMedCentralCrossRef
24.
go back to reference Kim HJ, Kim MJ, Ahn SH, Son BH, Kim SB, Ahn JH, Noh WC, Gong G: Different prognostic significance of CD24 and CD44 expression in breast cancer according to hormone receptor status. Breast. 2011, 20: 78-85. 10.1016/j.breast.2010.08.001.PubMedCrossRef Kim HJ, Kim MJ, Ahn SH, Son BH, Kim SB, Ahn JH, Noh WC, Gong G: Different prognostic significance of CD24 and CD44 expression in breast cancer according to hormone receptor status. Breast. 2011, 20: 78-85. 10.1016/j.breast.2010.08.001.PubMedCrossRef
25.
go back to reference Takahashi M, Nakajima M, Ogata H, Domeki Y, Ohtsuka K, Ihara K, Kurayama E, Yamaguchi S, Sasaki K, Miyachi K, Kato H: CD24 expression is associated with progression of gastric cancer. Hepatogastroenterology. 2013, 60: 653-658.PubMed Takahashi M, Nakajima M, Ogata H, Domeki Y, Ohtsuka K, Ihara K, Kurayama E, Yamaguchi S, Sasaki K, Miyachi K, Kato H: CD24 expression is associated with progression of gastric cancer. Hepatogastroenterology. 2013, 60: 653-658.PubMed
26.
go back to reference Yang XR, Xu Y, Yu B, Zhou J, Li JC, Qiu SJ, Shi YH, Wang XY, Dai Z, Shi GM, Wu B, Wu LM, Yang GH, Zhang BH, Qin WX, Fan J: CD24 is a novel predictor for poor prognosis of hepatocellular carcinoma after surgery. Clin Cancer Res. 2009, 15: 5518-5527. 10.1158/1078-0432.CCR-09-0151.PubMedCrossRef Yang XR, Xu Y, Yu B, Zhou J, Li JC, Qiu SJ, Shi YH, Wang XY, Dai Z, Shi GM, Wu B, Wu LM, Yang GH, Zhang BH, Qin WX, Fan J: CD24 is a novel predictor for poor prognosis of hepatocellular carcinoma after surgery. Clin Cancer Res. 2009, 15: 5518-5527. 10.1158/1078-0432.CCR-09-0151.PubMedCrossRef
27.
go back to reference Thomas S, Harding MA, Smith SC, Overdevest JB, Nitz MD, Frierson HF, Tomlins SA, Kristiansen G, Theodorescu D: CD24 is an effector of HIF-1-driven primary tumor growth and metastasis. Cancer Res. 2012, 72: 5600-5612. 10.1158/0008-5472.CAN-11-3666.PubMedPubMedCentralCrossRef Thomas S, Harding MA, Smith SC, Overdevest JB, Nitz MD, Frierson HF, Tomlins SA, Kristiansen G, Theodorescu D: CD24 is an effector of HIF-1-driven primary tumor growth and metastasis. Cancer Res. 2012, 72: 5600-5612. 10.1158/0008-5472.CAN-11-3666.PubMedPubMedCentralCrossRef
28.
go back to reference Zhu J, Zhang G, Lu H: CD24, COX-2, and p53 in epithelial ovarian cancer and its clinical significance. Front Biosci (Elite Ed). 2012, 4: 2745-2751. 10.2741/E580.CrossRef Zhu J, Zhang G, Lu H: CD24, COX-2, and p53 in epithelial ovarian cancer and its clinical significance. Front Biosci (Elite Ed). 2012, 4: 2745-2751. 10.2741/E580.CrossRef
29.
go back to reference Marmé F, Werft W, Walter A, Keller S, Wang X, Benner A, Burwinkel B, Sinn P, Hug S, Sohn C, Bretz N, Moldenhauer G, Rupp C, Rupp AK, Biakhov MY, Bottini A, Friedrichs K, Khailenko VA, Manikhas GM, Ruiz A, s'nchez-Rovira P, Santoro A, Segui MA, Villena C, Lichter P, Kristiansen G, Altevogt P, Schneeweiss A: CD24 Ala57Val polymorphism predicts pathologic complete response to sequential anthracycline- and taxane-based neoadjuvant chemotherapy for primary breast cancer. Breast Cancer Res Treat. 2011 In press. Marmé F, Werft W, Walter A, Keller S, Wang X, Benner A, Burwinkel B, Sinn P, Hug S, Sohn C, Bretz N, Moldenhauer G, Rupp C, Rupp AK, Biakhov MY, Bottini A, Friedrichs K, Khailenko VA, Manikhas GM, Ruiz A, s'nchez-Rovira P, Santoro A, Segui MA, Villena C, Lichter P, Kristiansen G, Altevogt P, Schneeweiss A: CD24 Ala57Val polymorphism predicts pathologic complete response to sequential anthracycline- and taxane-based neoadjuvant chemotherapy for primary breast cancer. Breast Cancer Res Treat. 2011 In press.
30.
go back to reference Liu C, Zheng S, Shen H, Xu K, Chen J, Li H, Xu Y, Xu A, Chen B, Kaku H, Nasu Y, Kumon H, Huang P, Watanabe M: Clinical significance of CD24 as a predictor of bladder cancer recurrence. Oncol Lett. 2013, 6: 96-100.PubMedPubMedCentral Liu C, Zheng S, Shen H, Xu K, Chen J, Li H, Xu Y, Xu A, Chen B, Kaku H, Nasu Y, Kumon H, Huang P, Watanabe M: Clinical significance of CD24 as a predictor of bladder cancer recurrence. Oncol Lett. 2013, 6: 96-100.PubMedPubMedCentral
31.
go back to reference Guo X, Xiong L, Zou L, Zhao J: Upregulation of bone morphogenetic protein 4 is associated with poor prognosis in patients with hepatocellular carcinoma. Pathol Oncol Res. 2012, 18: 635-640. 10.1007/s12253-011-9488-2.PubMedCrossRef Guo X, Xiong L, Zou L, Zhao J: Upregulation of bone morphogenetic protein 4 is associated with poor prognosis in patients with hepatocellular carcinoma. Pathol Oncol Res. 2012, 18: 635-640. 10.1007/s12253-011-9488-2.PubMedCrossRef
32.
go back to reference Guo X, Xiong L, Sun T, Peng R, Zou L, Zhu H, Zhang J, Li H, Zhao J: Expression features of SOX9 associate with tumor progression and poor prognosis of hepatocellular carcinoma. Diagn Pathol. 2012, 7: 44-10.1186/1746-1596-7-44.PubMedPubMedCentralCrossRef Guo X, Xiong L, Sun T, Peng R, Zou L, Zhu H, Zhang J, Li H, Zhao J: Expression features of SOX9 associate with tumor progression and poor prognosis of hepatocellular carcinoma. Diagn Pathol. 2012, 7: 44-10.1186/1746-1596-7-44.PubMedPubMedCentralCrossRef
33.
go back to reference Guo X, Xiong L, Zou L, Sun T, Zhang J, Li H, Peng R, Zhao J: L1 cell adhesion molecule overexpression in hepatocellular carcinoma associates with advanced tumor progression and poor patient survival. Diagn Pathol. 2012, 7: 96-10.1186/1746-1596-7-96.PubMedPubMedCentralCrossRef Guo X, Xiong L, Zou L, Sun T, Zhang J, Li H, Peng R, Zhao J: L1 cell adhesion molecule overexpression in hepatocellular carcinoma associates with advanced tumor progression and poor patient survival. Diagn Pathol. 2012, 7: 96-10.1186/1746-1596-7-96.PubMedPubMedCentralCrossRef
34.
go back to reference Gao L, Wu GJ, Liu XW, Zhang R, Yu L, Zhang G, Liu F, Yu CG, Yuan JL, Wang H, Yao LB: Suppression of invasion and metastasis of prostate cancer cells by overexpression of NDRG2 gene. Cancer Lett. 2011, 310: 94-100. 10.1016/j.canlet.2011.06.015.PubMedCrossRef Gao L, Wu GJ, Liu XW, Zhang R, Yu L, Zhang G, Liu F, Yu CG, Yuan JL, Wang H, Yao LB: Suppression of invasion and metastasis of prostate cancer cells by overexpression of NDRG2 gene. Cancer Lett. 2011, 310: 94-100. 10.1016/j.canlet.2011.06.015.PubMedCrossRef
35.
go back to reference Bircan S, Kapucuoglu N, Baspinar S, Inan G, Candir O: CD24 expression in ductal carcinoma in situ and invasive ductal carcinoma of breast: an immunohistochemistry-based pilot study. Pathol Res Pract. 2006, 202: 569-576. 10.1016/j.prp.2006.05.004.PubMedCrossRef Bircan S, Kapucuoglu N, Baspinar S, Inan G, Candir O: CD24 expression in ductal carcinoma in situ and invasive ductal carcinoma of breast: an immunohistochemistry-based pilot study. Pathol Res Pract. 2006, 202: 569-576. 10.1016/j.prp.2006.05.004.PubMedCrossRef
36.
go back to reference Purcell WT, Rudek MA, Hidalgo M: Development of matrix metalloproteinase inhibitors in cancer therapy. Hematol Oncol Clin North Am. 2002, 16: 1189-1227. 10.1016/S0889-8588(02)00044-8.PubMedCrossRef Purcell WT, Rudek MA, Hidalgo M: Development of matrix metalloproteinase inhibitors in cancer therapy. Hematol Oncol Clin North Am. 2002, 16: 1189-1227. 10.1016/S0889-8588(02)00044-8.PubMedCrossRef
37.
go back to reference Bendas G, Borsig L: Cancer cell adhesion and metastasis: selectins, integrins, and the inhibitory potential of heparins. Int J Cell Biol. 2012, 2012: 676731-10.1155/2012/676731.PubMedPubMedCentralCrossRef Bendas G, Borsig L: Cancer cell adhesion and metastasis: selectins, integrins, and the inhibitory potential of heparins. Int J Cell Biol. 2012, 2012: 676731-10.1155/2012/676731.PubMedPubMedCentralCrossRef
Metadata
Title
Combined aberrant expression of N-Myc downstream-regulated gene 2 and CD24 is associated with disease-free survival and overall survival in patients with hepatocellular carcinoma
Authors
Bing Li
Qing Shao
Dong Ji
Fan Li
Xiaodong Guo
Guofeng Chen
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Diagnostic Pathology / Issue 1/2014
Electronic ISSN: 1746-1596
DOI
https://doi.org/10.1186/s13000-014-0209-5

Other articles of this Issue 1/2014

Diagnostic Pathology 1/2014 Go to the issue