PI-88 inhibits postoperative recurrence of hepatocellular carcinoma via disrupting the surge of heparanase after liver resection

Tumor Biology

Volumn 37, Issue 3, 2016, Pages 2987-2998

  Liao, Bo Yi ^a   Wang, Zheng ^a   Hu, Jie ^a   Liu, Wei Feng ^a   Shen, Zao Zhuo ^a   Zhang, Xin ^a   Yu, Lei ^a   Fan, Jia ^a   Zhou, Jian ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

Adjuvant therapy; Heparanase; Hepatocellular carcinoma; PI 88; Recurrence

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; HEPARANASE; MUPARFOSTAT; BETA GLUCURONIDASE; OLIGOSACCHARIDE; PHOSPHOMANNOPENTAOSE SULFATE;

ANIMAL EXPERIMENT; ARTICLE; CANCER RECURRENCE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; LIVER RESECTION; MAJOR CLINICAL STUDY; MALE; METASTASIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; POLYMERASE CHAIN REACTION; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; TISSUE MICROARRAY; UPREGULATION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CARCINOMA, HEPATOCELLULAR; CELL MOTION; DRUG EFFECTS; ENZYMOLOGY; LIVER NEOPLASMS; PATHOLOGY; PHYSIOLOGY; PREVENTION AND CONTROL; SIGNAL TRANSDUCTION; TUMOR RECURRENCE;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL MOVEMENT; GLUCURONIDASE; HEPATECTOMY; LIVER NEOPLASMS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED BALB C; NEOPLASM RECURRENCE, LOCAL; OLIGOSACCHARIDES;

EID: 84944705855     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-015-4085-8     Document Type: Article

References (41)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63(1):11–30.
2. Maluccio M, Covey A. Recent progress in understanding, diagnosing, and treating hepatocellular carcinoma. CA Cancer J Clin. 2012;62(6):394–9.
3. Zhong JH, Ke Y, Gong WF, Xiang BD, Ma L, Ye XP, et al. Hepatic resection associated with good survival for selected patients with intermediate and advanced-stage hepatocellular carcinoma. Ann Surg. 2014;260(2):329–40.
4. Gluer AM, Cocco N, Laurence JM, Johnston ES, Hollands MJ, Pleass HC, et al. Systematic review of actual 10-year survival following resection for hepatocellular carcinoma. HPB (Oxford). 2012;14(5):285–90.
5. Zhong JH, Ma L, Li LQ. Postoperative therapy options for hepatocellular carcinoma. Scand J Gastroenterol. 2014;49(6):649–61.
6. Jeng WJ, Lin CC, Chen WT, Sheen IS, Lin CY, Lin SM. Adjuvant therapy for hepatocellular carcinoma after curative treatment. Dig Dis. 2014;32(6):747–54.
7. Barker HE, Chang J, Cox TR, Lang G, Bird D, Nicolau M, et al. LOXL2-mediated matrix remodeling in metastasis and mammary gland involution. Cancer Res. 2011;71(5):1561–72.
8. Zhang YF, Tang XD, Gao JH, Fang DC, Yang SM. Heparanase: a universal immunotherapeutic target in human cancers. Drug Discov Today. 2011;16(9–10):412–7.
9. Talmadge JE, Fidler IJ. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res. 2010;70(14):5649–69.
10. Vlodavsky I, Friedmann Y. Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J Clin Invest. 2001;108(3):341–7.
11. Yuan SX, Yang F, Yang Y, Tao QF, Zhang J, Huang G, et al. Long noncoding RNA associated with microvascular invasion in hepatocellular carcinoma promotes angiogenesis and serves as a predictor for hepatocellular carcinoma patients’ poor recurrence-free survival after hepatectomy. Hepatology. 2012;56(6):2231–41.
12. Meirovitz A, Hermano E, Lerner I, Zcharia E, Pisano C, Peretz T, et al. Role of heparanase in radiation-enhanced invasiveness of pancreatic carcinoma. Cancer Res. 2011;71(7):2772–80.
13. Marchetti D, McQuillan DJ, Spohn WC, Carson DD, Nicolson GL. Neurotrophin stimulation of human melanoma cell invasion: selected enhancement of heparanase activity and heparanase degradation of specific heparan sulfate subpopulations. Cancer Res. 1996;56(12):2856–63.
14. Ogishima T, Shiina H, Breault JE, Terashima M, Honda S, Enokida H, et al. Promoter CpG hypomethylation and transcription factor EGR1 hyperactivate heparanase expression in bladder cancer. Oncogene. 2005;24(45):6765–72.
15. Ogishima T, Shiina H, Breault JE, Tabatabai L, Bassett WW, Enokida H, et al. Increased heparanase expression is caused by promoter hypomethylation and up-regulation of transcriptional factor early growth response-1 in human prostate cancer. Clin Cancer Res. 2005;11(3):1028–36.
16. Liu CJ, Lee PH, Lin DY, Wu CC, Jeng LB, Lin PW, et al. Heparanase inhibitor PI-88 as adjuvant therapy for hepatocellular carcinoma after curative resection: a randomized phase II trial for safety and optimal dosage. J Hepatol. 2009;50(5):958–68.
17. Yang BW, Liang Y, Xia JL, Sun HC, Wang L, Zhang JB, et al. Biological characteristics of fluorescent protein-expressing human hepatocellular carcinoma xenograft model in nude mice. Eur J Gastroenterol Hepatol. 2008;20(11):1077–84.
18. Gao Q, Qiu SJ, Fan J, Zhou J, Wang XY, Xiao YS, et al. Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol. 2007;25(18):2586–93.
19. Zhu K, Dai Z, Pan Q, Wang Z, Yang GH, Yu L, et al. Metadherin promotes hepatocellular carcinoma metastasis through induction of epithelial-mesenchymal transition. Clin Cancer Res. 2011;17(23):7294–302.
20. Lerner I, Baraz L, Pikarsky E, Meirovitz A, Edovitsky E, Peretz T, et al. Function of heparanase in prostate tumorigenesis: potential for therapy. Clin Cancer Res. 2008;14(3):668–76.
21. Zhang W, Zhu XD, Sun HC, Xiong YQ, Zhuang PY, Xu HX, et al. Depletion of tumor-associated macrophages enhances the effect of sorafenib in metastatic liver cancer models by antimetastatic and antiangiogenic effects. Clin Cancer Res. 2010;16(13):3420–30.
22. Fausto N. Liver regeneration. J Hepatol. 2000;32(1 Suppl):19–31.
23. Seki E, Kondo Y, Iimuro Y, Naka T, Son G, Kishimoto T, et al. Demonstration of cooperative contribution of MET- and EGFR-mediated STAT3 phosphorylation to liver regeneration by exogenous suppressor of cytokine signalings. J Hepatol. 2008;48(2):237–45.
24. Gao L, Utsumi T, Tashiro K, Liu B, Zhang D, Swenson ES, et al. Reticulon 4B (Nogo-B) facilitates hepatocyte proliferation and liver regeneration in mice. Hepatology. 2013;57(5):1992–2003.
25. de Mestre AM, Rao S, Hornby JR, Soe-Htwe T, Khachigian LM, Hulett MD. Early growth response gene 1 (EGR1) regulates heparanase gene transcription in tumor cells. J Biol Chem. 2005;280(42):35136–47.
26. Ferraro B, Bepler G, Sharma S, Cantor A, Haura EB. EGR1 predicts PTEN and survival in patients with non-small-cell lung cancer. J Clin Oncol. 2005;23(9):1921–6.
27. Mei Y, Thevananther S. Endothelial nitric oxide synthase is a key mediator of hepatocyte proliferation in response to partial hepatectomy in mice. Hepatology. 2011;54(5):1777–89.
28. Dussmann P, Pagel JI, Vogel S, Magnusson T, Zimmermann R, Wagner E, et al. Live in vivo imaging of Egr-1 promoter activity during neonatal development, liver regeneration and wound healing. BMC Dev Biol. 2011;11:28.
29. Poon RT. Prevention of recurrence after resection of hepatocellular carcinoma: a daunting challenge. Hepatology. 2011;54(3):757–9.
30. Neaud V, Faouzi S, Guirouilh J, Le Bail B, Balabaud C, Bioulac-Sage P, et al. Human hepatic myofibroblasts increase invasiveness of hepatocellular carcinoma cells: evidence for a role of hepatocyte growth factor. Hepatology. 1997;26(6):1458–66.
31. Worden B, Yang XP, Lee TL, Bagain L, Yeh NT, Cohen JG, et al. Hepatocyte growth factor/scatter factor differentially regulates expression of proangiogenic factors through Egr-1 in head and neck squamous cell carcinoma. Cancer Res. 2005;65(16):7071–80.
32. Lerner I, Hermano E, Zcharia E, Rodkin D, Bulvik R, Doviner V, et al. Heparanase powers a chronic inflammatory circuit that promotes colitis-associated tumorigenesis in mice. J Clin Invest. 2011;121(5):1709–21.
33. Carmel J, Arish A, Shoshany G, Baruch Y. Heparanase accelerates the proliferation of both hepatocytes and endothelial cells early after partial hepatectomy. Exp Mol Pathol. 2012;92(2):202–9.
34. Goldshmidt O, Yeikilis R, Mawasi N, Paizi M, Gan N, Ilan N, et al. Heparanase expression during normal liver development and following partial hepatectomy. J Pathol. 2004;203(1):594–602.
35. Cohen E, Doweck I, Naroditsky I, Ben-Izhak O, Kremer R, Best LA, et al. Heparanase is overexpressed in lung cancer and correlates inversely with patient survival. Cancer. 2008;113(5):1004–11.
36. Ben-Izhak O, Kaplan-Cohen V, Ilan N, Gan S, Vlodavsky I, Nagler R. Heparanase expression in malignant salivary gland tumors inversely correlates with long-term survival. Neoplasia. 2006;8(10):879–84.
37. Riaz A, Ilan N, Vlodavsky I, Li JP, Johansson S. Characterization of heparanase-induced phosphatidylinositol 3-kinase-AKT activation and its integrin dependence. J Biol Chem. 2013;288(17):12366–75.
38. Zetser A, Bashenko Y, Edovitsky E, Levy-Adam F, Vlodavsky I, Ilan N. Heparanase induces vascular endothelial growth factor expression: correlation with p38 phosphorylation levels and Src activation. Cancer Res. 2006;66(3):1455–63.
39. Purushothaman A, Babitz SK, Sanderson RD. Heparanase enhances the insulin receptor signaling pathway to activate extracellular signal-regulated kinase in multiple myeloma. J Biol Chem. 2012;287(49):41288–96.
40. Joyce JA, Freeman C, Meyer-Morse N, Parish CR, Hanahan D. A functional heparan sulfate mimetic implicates both heparanase and heparan sulfate in tumor angiogenesis and invasion in a mouse model of multistage cancer. Oncogene. 2005;24(25):4037–51.
41. Johnstone KD, Karoli T, Liu L, Dredge K, Copeman E, Li CP, et al. Synthesis and biological evaluation of polysulfated oligosaccharide glycosides as inhibitors of angiogenesis and tumor growth. J Med Chem. 2010;53(4):1686–99.