The glypican 3 hepatocellular carcinoma marker regulates human hepatic stellate cells via Hedgehog signaling

Journal of Surgical Research

Volumn 187, Issue 2, 2014, Pages 377-385

  Magistri, Paolo ^a,b   Leonard, Stephanie Y ^a   Tang, Chih Min ^a   Chan, Jonathan C ^a   Lee, Tracy E ^a   Sicklick, Jason K ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Epithelial mesenchymal interactions; GPC3; HCC; Hedgehog interacting protein; Hepatoma; HSC; Tumor stroma interactions

Indexed keywords

GLYPICAN 3; HEPARIN; MESSENGER RNA; RECOMBINANT PROTEIN; SONIC HEDGEHOG PROTEIN; TUMOR MARKER;

APOPTOSIS ASSAY; ARTICLE; CELL VIABILITY; COCULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL CARCINOMA; PARACRINE SIGNALING; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STELLATE CELL;

EPITHELIAL-MESENCHYMAL INTERACTIONS; GPC3; HCC; HEDGEHOG-INTERACTING PROTEIN; HEPATOMA; HSC; TUMOR-STROMA INTERACTIONS;

ANTICOAGULANTS; APOPTOSIS; BINDING, COMPETITIVE; CARCINOMA, HEPATOCELLULAR; CARRIER PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; EUKARYOTIC INITIATION FACTOR-3; GLYPICANS; HEPARIN; HEPATIC STELLATE CELLS; HUMANS; LIVER NEOPLASMS; MEMBRANE GLYCOPROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84900538796     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2013.12.010     Document Type: Article

References (47)

1. H.B. El-Serag, and K.L. Rudolph Hepatocellular carcinoma: epidemiology and molecular carcinogenesis Gastroenterology 132 2007 2557
2. H.B. El-Serag Hepatocellular carcinoma: recent trends in the United States Gastroenterology 127 5 Suppl 1 2004 S27
3. H.B. El-Serag Epidemiology of hepatocellular carcinoma in USA Hepatol Res 37 Suppl 2 2007 S88
4. M.S. Ascha, I.A. Hanouneh, R. Lopez, T.A. Tamimi, A.F. Feldstein, and N.N. Zein The incidence and risk factors of hepatocellular carcinoma in patients with nonalcoholic steatohepatitis Hepatology 51 2010 1972
5. J.M. Clark, and A.M. Diehl Nonalcoholic fatty liver disease: an underrecognized cause of cryptogenic cirrhosis JAMA 289 2003 3000
6. J.K. Sicklick Correcting the misnomers of epithelial-mesenchymal relations J Surg Res 2012
7. K.P. Olive, M.A. Jacobetz, and C.J. Davidson et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer Science 324 2009 1457
8. A. Mazzocca, E. Fransvea, F. Dituri, L. Lupo, S. Antonaci, and G. Giannelli Down-regulation of connective tissue growth factor by inhibition of transforming growth factor beta blocks the tumor-stroma cross-talk and tumor progression in hepatocellular carcinoma Hepatology 51 2010 523
9. T. Amann, F. Bataille, and T. Spruss et al. Activated hepatic stellate cells promote tumorigenicity of hepatocellular carcinoma Cancer Sci 100 2009 646
10. C. Coulouarn, A. Corlu, D. Glaise, I. Guenon, S.S. Thorgeirsson, and B. Clement Hepatocyte-stellate cell cross-talk in the liver engenders a permissive inflammatory microenvironment that drives progression in hepatocellular carcinoma Cancer Res 72 2012 2533
11. P. Sancho-Bru, E. Juez, and M. Moreno et al. Hepatocarcinoma cells stimulate the growth, migration and expression of pro-angiogenic genes in human hepatic stellate cells Liver Int 30 2010 31
12. I.S. Chan, C.D. Guy, and Y. Chen et al. Paracrine Hedgehog signaling drives metabolic changes in hepatocellular carcinoma Cancer Res 72 2012 6344
13. J.K. Sicklick, Y.X. Li, and S.S. Choi et al. Role for hedgehog signaling in hepatic stellate cell activation and viability Lab Invest 85 2005 1368
14. S.S. Choi, A. Omenetti, and R.P. Witek et al. Hedgehog pathway activation and epithelial-to-mesenchymal transitions during myofibroblastic transformation of rat hepatic cells in culture and cirrhosis Am J Physiol Gastrointest Liver Physiol 297 2009 G1093
15. J.K. Sicklick, Y.X. Li, and A. Melhem et al. Hedgehog signaling maintains resident hepatic progenitors throughout life Am J Physiol Gastrointest Liver Physiol 290 2006 G859
16. R.P. Witek, L. Yang, and R. Liu et al. Liver cell-derived microparticles activate hedgehog signaling and alter gene expression in hepatic endothelial cells Gastroenterology 136 2009 320
17. L. Yang, Y. Wang, and H. Mao et al. Sonic hedgehog is an autocrine viability factor for myofibroblastic hepatic stellate cells J Hepatol 48 2008 98
18. A. Omenetti, W.K. Syn, and Y. Jung et al. Repair-related activation of hedgehog signaling promotes cholangiocyte chemokine production Hepatology 50 2009 518
19. J.K. Sicklick, Y.X. Li, and A. Jayaraman et al. Dysregulation of the Hedgehog pathway in human hepatocarcinogenesis Carcinogenesis 27 2006 748
20. M.A. Patil, J. Zhang, C. Ho, S.T. Cheung, S.T. Fan, and X. Chen Hedgehog signaling in human hepatocellular carcinoma Cancer Biol Ther 5 2006 111
21. A. Gallet, L. Staccini-Lavenant, and P.P. Therond Cellular trafficking of the glypican Dally-like is required for full-strength Hedgehog signaling and wingless transcytosis Dev Cell 14 2008 712
22. M. Capurro, I.R. Wanless, and M. Sherman et al. Glypican-3: a novel serum and histochemical marker for hepatocellular carcinoma Gastroenterology 125 2003 89
23. Y. Midorikawa, S. Ishikawa, and H. Iwanari et al. Glypican-3, overexpressed in hepatocellular carcinoma, modulates FGF2 and BMP-7 signaling Int J Cancer 103 2003 455
24. M.I. Capurro, P. Xu, W. Shi, F. Li, A. Jia, and J. Filmus et al. Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding Dev Cell 14 2008 700
25. D. Yan, and X. Lin Opposing roles for glypicans in Hedgehog signalling Nat Cell Biol 10 2008 761
26. G. Pilia, R.M. Hughes-Benzie, and A. MacKenzie et al. Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome Nat Genet 12 1996 241
27. C.W. Lin, W.M. Mars, and S. Paranjpe et al. Hepatocyte proliferation and hepatomegaly induced by phenobarbital and 1,4-bis [2-(3,5-dichloropyridyloxy)] benzene is suppressed in hepatocyte-targeted glypican 3 transgenic mice Hepatology 54 2011 620
28. B. Liu, A.W. Bell, and S. Paranjpe et al. Suppression of liver regeneration and hepatocyte proliferation in hepatocyte-targeted glypican 3 transgenic mice Hepatology 52 2010 1060
29. X.Y. Wang, F. Degos, and S. Dubois et al. Glypican-3 expression in hepatocellular tumors: diagnostic value for preneoplastic lesions and hepatocellular carcinomas Hum Pathol 37 2006 1435
30. H. Shirakawa, H. Suzuki, and M. Shimomura et al. Glypican-3 expression is correlated with poor prognosis in hepatocellular carcinoma Cancer Sci 100 2009 1403
31. L. Xu, A.Y. Hui, and E. Albanis et al. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis Gut 54 2005 142
32. A. Omenetti, L. Yang, and Y.X. Li et al. Hedgehog-mediated mesenchymal-epithelial interactions modulate hepatic response to bile duct ligation Lab Invest 87 2007 499
33. T. Nakatsura, Y. Yoshitake, and S. Senju et al. Glypican-3, overexpressed specifically in human hepatocellular carcinoma, is a novel tumor marker Biochem Biophys Res Commun 306 2003 16
34. M. Tada, F. Kanai, and Y. Tanaka et al. Down-regulation of hedgehog-interacting protein through genetic and epigenetic alterations in human hepatocellular carcinoma Clin Cancer Res 14 2008 3768
35. A. Omenetti, Y. Popov, and Y. Jung et al. The hedgehog pathway regulates remodelling responses to biliary obstruction in rats Gut 57 2008 1275
36. C.L. Olsen, P.P. Hsu, J. Glienke, G.M. Rubanyi, and A.R. Brooks Hedgehog-interacting protein is highly expressed in endothelial cells but down-regulated during angiogenesis and in several human tumors BMC Cancer 4 2004 43
37. B. Liu, S. Paranjpe, and W.C. Bowen et al. Investigation of the role of glypican 3 in liver regeneration and hepatocyte proliferation Am J Pathol 175 2009 717
38. M.J. Ju, S.J. Qiu, and J. Fan et al. Peritumoral activated hepatic stellate cells predict poor clinical outcome in hepatocellular carcinoma after curative resection Am J Clin Pathol 131 2009 498
39. M. Suzuki, K. Sugimoto, and J. Tanaka et al. Up-regulation of glypican-3 in human hepatocellular carcinoma Anticancer Res 30 2010 5055
40. K. Yorita, N. Takahashi, and H. Takai et al. Prognostic significance of circumferential cell surface immunoreactivity of glypican-3 in hepatocellular carcinoma Liver Int 31 2011 120
41. D.D. Yu, M. Yao, and J. Chen et al. [Short hairpin RNA mediated glypican-3 silencing inhibits hepatoma cell invasiveness and disrupts molecular pathways of angiogenesis] Zhonghua Gan Zang Bing Za Zhi 21 2013 452
42. S.I. Zittermann, M.I. Capurro, W. Shi, and J. Filmus Soluble glypican 3 inhibits the growth of hepatocellular carcinoma in vitro and in vivo Int J Cancer 126 2010 1291
43. T. Roskams, J. Rosenbaum, R. De Vos, G. David, and V. Desmet et al. Heparan sulfate proteoglycan expression in chronic cholestatic human liver diseases Hepatology 24 1996 524
44. S.L. Friedman Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver Physiol Rev 88 2008 125
45. M. Ho Advances in liver cancer antibody therapies: a focus on glypican-3 and mesothelin BioDrugs 25 2011 275
46. Y. Motomura, Y. Ikuta, and T. Kuronuma et al. HLA-A2 and -A24-restricted glypican-3-derived peptide vaccine induces specific CTLs: preclinical study using mice Int J Oncol 32 2008 985
47. T. Ishiguro, M. Sugimoto, and Y. Kinoshita et al. Anti-glypican 3 antibody as a potential antitumor agent for human liver cancer Cancer Res 68 2008 9832