Human monoclonal antibody targeting the heparan sulfate chains of Glypican-3 inhibits HGF-mediated migration and motility of hepatocellular carcinoma cells

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Gao, Wei ^a   Kim, Heungnam ^a   Ho, Mitchell ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORE PROTEIN; GLYPICAN 3; HEPARAN SULFATE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY HS20; MUTANT PROTEIN; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; WNT PROTEIN; GLYPICAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN ANTIBODY REACTION; ARTICLE; CANCER INHIBITION; CARCINOMA CELL; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; LIVER TUMOR; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR SPHEROID; WNT SIGNALING PATHWAY; CELL MOTION; CHEMISTRY; IMMUNOLOGY; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANTIBODIES, MONOCLONAL; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL MOVEMENT; GLYPICANS; HEPARITIN SULFATE; HEPATOCYTE GROWTH FACTOR; HUMANS; LIVER NEOPLASMS;

EID: 84947589959     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137664     Document Type: Article

References (46)

1. Akutsu N, Yamamoto H, Sasaki S, Taniguchi H, Arimura Y, Imai K, et al. (2010) Association of glypican- 3 expression with growth signaling molecules in hepatocellular carcinoma. World J Gastroenterol 16: 3521-3528. PMID: 20653060
2. Perini MV, Starkey G, Fink MA, Bhandari R, Muralidharan V, Jones R, et al. (2015) From minimal to maximal surgery in the treatment of hepatocarcinoma: A review. World J Hepatol 7: 93-100. doi: 10.4254/wjh.v7.i1.93 PMID: 25625000
3. Bruix J, Gores GJ, Mazzaferro V (2014) Hepatocellular carcinoma: clinical frontiers and perspectives. Gut 63: 844-855. doi: 10.1136/gutjnl-2013-306627 PMID: 24531850
4. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, et al. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68: 729-777. PMID: 10872465
5. Sasisekharan R, Shriver Z, Venkataraman G, Narayanasami U (2002) Roles of heparan-sulphate glycosaminoglycans in cancer. Nat Rev Cancer 2: 521-528. PMID: 12094238
6. Filmus J, Capurro M, Rast J (2008) Glypicans. Genome Biol 9: 224. doi: 10.1186/gb-2008-9-5-224 PMID: 18505598
7. Hsu HC, Cheng W, Lai PL (1997) Cloning and expression of a developmentally regulated transcript MXR7 in hepatocellular carcinoma: biological significance and temporospatial distribution. Cancer Res 57: 5179-5184. PMID: 9371521
8. Shirakawa H, Suzuki H, Shimomura M, Kojima M, Gotohda N, Takahashi S, et al. (2009) Glypican-3 expression is correlated with poor prognosis in hepatocellular carcinoma. Cancer Sci 100: 1403-1407. doi: 10.1111/j.1349-7006.2009.01206.x PMID: 19496787
9. Gao W, Kim H, Feng M, Phung Y, Xavier CP, Rubin JS, et al. (2014) Inactivation of Wnt signaling by a human antibody that recognizes the heparan sulfate chains of glypican-3 for liver cancer therapy. Hepatology 60: 576-587. doi: 10.1002/hep.26996 PMID: 24492943
10. Capurro MI, Xiang YY, Lobe C, Filmus J (2005) Glypican-3 promotes the growth of hepatocellular carcinoma by stimulating canonical Wnt signaling. Cancer Res 65: 6245-6254. PMID: 16024626
11. Feng M, Gao W, Wang R, Chen W, Man YG, Figg WD, et al. (2013) Therapeutically targeting glypican- 3 via a conformation-specific single-domain antibody in hepatocellular carcinoma. Proc Natl Acad Sci U S A 110: E1083-1091. doi: 10.1073/pnas.1217868110 PMID: 23471984
12. Giordano S, Columbano A (2014) Met as a therapeutic target in HCC: facts and hopes. J Hepatol 60: 442-452. doi: 10.1016/j.jhep.2013.09.009 PMID: 24045150
13. Amicone L, Spagnoli FM, Spath G, Giordano S, Tommasini C, Bernardini S, et al. (1997) Transgenic expression in the liver of truncated Met blocks apoptosis and permits immortalization of hepatocytes. EMBO J 16: 495-503. PMID: 9034332
14. Huh CG, Factor VM, Sanchez A, Uchida K, Conner EA, Thorgeirsson SS (2004) Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci U S A 101: 4477-4482. PMID: 15070743
15. Borowiak M, Garratt AN, Wustefeld T, Strehle M, Trautwein C, Birchmeier C (2004) Met provides essential signals for liver regeneration. Proc Natl Acad Sci U S A 101: 10608-10613. PMID: 15249655
16. Uehara Y, Minowa O, Mori C, Shiota K, Kuno J, Noda T, et al. (1995) Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373: 702-705. PMID: 7854453
17. Schmidt C, Bladt F, Goedecke S, Brinkmann V, Zschiesche W, Sharpe M, et al. (1995) Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373: 699-702. PMID: 7854452
18. Ueki T, Fujimoto J, Suzuki T, Yamamoto H, Okamoto E (1997) Expression of hepatocyte growth factor and its receptor c-met proto-oncogene in hepatocellular carcinoma. Hepatology 25: 862-866. PMID: 9096589
19. Boccaccio C, Comoglio PM (2006) Invasive growth: a MET-driven genetic programme for cancer and stem cells. Nat Rev Cancer 6: 637-645. PMID: 16862193
20. Kaposi-Novak P, Lee JS, Gomez-Quiroz L, Coulouarn C, Factor VM, Thorgeirsson SS (2006) Met-regulated expression signature defines a subset of human hepatocellular carcinomas with poor prognosis and aggressive phenotype. J Clin Invest 116: 1582-1595. PMID: 16710476
21. Llovet JM, Hernandez-Gea V (2014) Hepatocellular carcinoma: reasons for phase III failure and novel perspectives on trial design. Clin Cancer Res 20: 2072-2079. doi: 10.1158/1078-0432.CCR-13-0547 PMID: 24589894
22. Venero Galanternik M, Kramer KL, Piotrowski T (2015) Heparan Sulfate Proteoglycans Regulate Fgf Signaling and Cell Polarity during Collective Cell Migration. Cell Rep.
23. Derksen PW, Keehnen RM, Evers LM, van Oers MH, Spaargaren M, Pals ST (2002) Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma. Blood 99: 1405-1410. PMID: 11830493
24. Cecchi F, Pajalunga D, Fowler CA, Uren A, Rabe DC, Peruzzi B, et al. (2012) Targeted disruption of heparan sulfate interaction with hepatocyte and vascular endothelial growth factors blocks normal and oncogenic signaling. Cancer Cell 22: 250-262. doi: 10.1016/j.ccr.2012.06.029 PMID: 22897854
25. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J (1982) Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42: 3858-3863. PMID: 6286115
26. Ho M, Kreitman RJ, Onda M, Pastan I (2005) In vitro antibody evolution targeting germline hot spots to increase activity of an anti-CD22 immunotoxin. J Biol Chem 280: 607-617. PMID: 15491997
27. Phung Y, Gao W, Man YG, Nagata S, Ho M (2012) High-affinity monoclonal antibodies to cell surface tumor antigen glypican-3 generated through a combination of peptide immunization and flow cytometry screening. MAbs 4: 592-599. doi: 10.4161/mabs.20933 PMID: 22820551
28. Geback T, Schulz MM, Koumoutsakos P, Detmar M (2009) TScratch: a novel and simple software tool for automated analysis of monolayer wound healing assays. Biotechniques 46: 265-274. doi: 10.2144/000113083 PMID: 19450233
29. Gutierrez J, Cabrera D, Brandan E (2014) Glypican-1 regulates myoblast response to HGF via Met in a lipid raft-dependent mechanism: effect on migration of skeletal muscle precursor cells. Skelet Muscle 4: 5. doi: 10.1186/2044-5040-4-5 PMID: 24517345
30. Karihaloo A, Kale S, Rosenblum ND, Cantley LG (2004) Hepatocyte growth factor-mediated renal epithelial branching morphogenesis is regulated by glypican-4 expression. Mol Cell Biol 24: 8745-8752. PMID: 15367691
31. Weiswald LB, Bellet D, Dangles-Marie V (2015) Spherical Cancer Models in Tumor Biology. Neoplasia 17: 1-15. doi: 10.1016/j.neo.2014.12.004 PMID: 25622895
32. de La Coste A, Romagnolo B, Billuart P, Renard CA, Buendia MA, Soubrane O, et al. (1998) Somatic mutations of the beta-catenin gene are frequent in mouse and human hepatocellular carcinomas. Proc Natl Acad Sci U S A 95: 8847-8851. PMID: 9671767
33. Sanderson RD (2001) Heparan sulfate proteoglycans in invasion and metastasis. Semin Cell Dev Biol 12: 89-98. PMID: 11292374
34. Parish CR, Freeman C, Brown KJ, Francis DJ, Cowden WB (1999) Identification of sulfated oligosaccharide-based inhibitors of tumor growth and metastasis using novel in vitro assays for angiogenesis and heparanase activity. Cancer Res 59: 3433-3441. PMID: 10416607
35. Ferro V, Dredge K, Liu L, Hammond E, Bytheway I, Li C, et al. (2007) PI-88 and novel heparan sulfate mimetics inhibit angiogenesis. Semin Thromb Hemost 33: 557-568. PMID: 17629854
36. Kudchadkar R, Gonzalez R, Lewis KD (2008) PI-88: a novel inhibitor of angiogenesis. Expert Opin Investig Drugs 17: 1769-1776. doi: 10.1517/13543784.17.11.1769 PMID: 18922112
37. Liu CJ, Lee PH, Lin DY, Wu CC, Jeng LB, Lin PW, et al. (2009) 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 50: 958-968. doi: 10.1016/j.jhep.2008.12.023 PMID: 19303160
38. Ferro V, Liu L, Johnstone KD, Wimmer N, Karoli T, Handley P, et al. (2012) Discovery of PG545: a highly potent and simultaneous inhibitor of angiogenesis, tumor growth, and metastasis. J Med Chem 55: 3804-3813. doi: 10.1021/jm201708h PMID: 22458531
39. Gerotziafas GT, Papageorgiou C, Hatmi M, Samama MM, Elalamy I (2008) Clinical studies with anticoagulants to improve survival in cancer patients. Pathophysiol Haemost Thromb 36: 204-211. doi: 10.1159/000175158 PMID: 19176993
40. Sarrazin S, Lamanna WC, Esko JD (2011) Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol 3.
41. Gao W, Tang Z, Zhang YF, Feng M, Qian M, Dimitrov DS, et al. (2015) Immunotoxin targeting glypican- 3 regresses liver cancer via dual inhibition of Wnt signalling and protein synthesis. Nat Commun 6: 6536. doi: 10.1038/ncomms7536 PMID: 25758784
42. Aikawa T, Whipple CA, Lopez ME, Gunn J, Young A, Lander AD, et al. (2008) Glypican-1 modulates the angiogenic and metastatic potential of human and mouse cancer cells. J Clin Invest 118: 89-99. PMID: 18064304
43. Kayed H, Kleeff J, Keleg S, Jiang X, Penzel R, Giese T, et al. (2006) Correlation of glypican-1 expression with TGF-beta, BMP, and activin receptors in pancreatic ductal adenocarcinoma. Int J Oncol 29: 1139-1148. PMID: 17016645
44. Orentas RJ, Yang JJ, Wen X, Wei JS, Mackall CL, Khan J (2012) Identification of cell surface proteins as potential immunotherapy targets in 12 pediatric cancers. Front Oncol 2: 194. doi: 10.3389/fonc. 2012.00194 PMID: 23251904
45. Li F, Shi W, Capurro M, Filmus J (2011) Glypican-5 stimulates rhabdomyosarcoma cell proliferation by activating Hedgehog signaling. J Cell Biol 192: 691-704. doi: 10.1083/jcb.201008087 PMID: 21339334
46. Williamson D, Selfe J, Gordon T, Lu YJ, Pritchard-Jones K, Murai K, et al. (2007) Role for amplification and expression of glypican-5 in rhabdomyosarcoma. Cancer Res 67: 57-65. PMID: 17210683