Heparin inhibits Hepatocyte growth factor induced motility and invasion of hepatocellular carcinoma cells through early growth response protein 1

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Ozen, Evin ^a   Gozukizil, Aysim ^a   Erdal, Esra ^a   Uren, Aykut ^b   Bottaro, Donald P ^c   Atabey, Nese ^a  

^a DOKUZ EYLUL UNIVERSITY   (Turkey)

^b GEORGETOWN UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; GELATINASE A; GELATINASE B; HEPARIN; MATRIX METALLOPROTEINASE 14; MITOGEN ACTIVATED PROTEIN KINASE; SCATTER FACTOR; SCATTER FACTOR RECEPTOR;

ARTICLE; CARCINOMA CELL; CELL ADHESION; CELL INVASION; CELL MOTILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; METASTASIS INHIBITION; MIGRATION INHIBITION; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION;

CARCINOMA, HEPATOCELLULAR; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; EARLY GROWTH RESPONSE PROTEIN 1; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HEPARIN; HEPATOCYTE GROWTH FACTOR; HUMANS; INDOLES; LIVER NEOPLASMS; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM INVASIVENESS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-MET; SULFONAMIDES; TRANSCRIPTION, GENETIC;

EID: 84865060044     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042717     Document Type: Article

References (61)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, et al. (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127: 2893-917 doi: 10.1002/ijc.25516.
2. Livraghi T, Mäkisalo H, Line PD, (2011) Treatment options in hepatocellular carcinoma today. Scand J Surg 100: 22-9.
3. Zhang ZM, Guo JX, Zhang ZC, Jiang N, Zhang ZY, et al. (2011) Therapeutic options for intermediate-advanced hepatocellular carcinoma. World J Gastroenterol 17: 1685-9.
4. You H, Ding W, Dang H, Jiang Y, Rountree CB, (2011) c- Met represents a potential therapeutic target for personalized treatment in hepatocellular carcinoma. Hepatology 54: 879-89 doi: 10.1002/hep.24450.
5. Kaposi-Novak P, Lee JS, Gòmez-Quiroz L, Coulouarn C, Factor VM, et al. (2006) Met-regulated expression signature defines a subset of human hepatocellular carcinomas with poor prognosis and aggressive phenotype. J Clin Invest 116: 1582-95.
6. Severi T, van Malenstein H, Verslype C, van Pelt JF, (2010) Tumor initiation and progression in hepatocellular carcinoma: risk factors, classification, and therapeutic targets. Acta Pharmacol Sin 31: 1409-20.
7. van Malenstein H, van Pelt J, Verslype C, (2011) Molecular classification of hepatocellular carcinoma anno 2011. Eur J Cancer 47: 1789-97.
8. Whittaker S, Marais R, Zhu AX, (2010) The role of signaling pathways in the development and treatment of hepatocellular carcinoma. Oncogene 29: 4989-5005.
9. Nagai T, Arao T, Furuta K, Sakai K, Kudo K, et al. (2011) Sorafenib inhibits the hepatocyte growth factor-mediated epithelial mesenchymal transition in hepatocellular carcinoma. Mol Cancer Ther 10: 169-77.
10. Henry JC, Park JK, Jiang J, Kim JH, Nagorney DM, et al. (2010) miR-199a-3p targets CD44 and reduces proliferation of CD44 positive hepatocellular carcinoma cell lines. Biochem Biophys Res Commun 403: 120-5.
11. Boccaccio C, Comoglio PM, (2006) Invasive growth: a MET-driven genetic programme for cancer and stemcells. Nat Rev Cancer 8: 637-45.
12. Marx-Stoelting P, Borowiak M, Knorpp T, Birchmeier C, Buchmann A, et al. (2009) Hepatocarcinogenesis in mice with a conditional knockout of the hepatocyte growth factor receptor c-Met. Int J Cancer 124: 1767-72.
13. Sakata H, Stahl SJ, Taylor WG, Rosenberg JM, Sakaguchi K, et al. (1997) Heparin binding and oligomerization of hepatocyte growth factor/scatter factor isoforms. Heparan sulfate glycosaminoglycan requirement for Met binding and signaling. J Biol Chem 272: 9457-63.
14. Deakin JA, Lyon M, (1999) Differential regulation of hepatocyte growth factor/scatter factor by cell surface proteoglycans and free glycosaminoglycan chains. J Cell Sci 112: 1999-2009.
15. Lyon M, Deakin JA, Gallagher JT, (2002) The mode of action of heparan and dermatan sulfates in the regulation of hepatocyte growth factor/scatter factor. J Biol Chem 277: 1040-6.
16. Rubin JS, Day RM, Breckenridge D, Atabey N, Taylor WG, et al. (2001) Dissociation of heparan sulfate and receptor binding domains of hepatocyte growth factor reveals that heparan sulfate-c-met interaction facilitates signaling. J Biol Chem 276: 32977-83.
17. Lai JP, Chien J, Strome SE, Staub J, Montoya DP, et al. (2004) HSulf-1 modulates HGF-mediated tumor cell invasion and signaling in head and neck squamous carcinoma. Oncogene 23: 1439-47.
18. Nagy Z, Turcsik V, Blaskó G, (2009) The Effect of LMWH (Nadroparin) on tumor progression. Pathol and Oncol Res 15: 689-692.
19. Ritchie JP, Ramani VC, Ren Y, Naggi A, Torri G, et al. (2011) SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis. Clin Cancer Res 17: 1382-93.
20. Borsig L, (2010) Antimetastatic activities of heparins and modified heparins. Experimental evidence. Thromb Res 2: S66-S71.
21. van Doormaal FF, Di Nisio M, Otten HM, Richel DJ, Prins M, et al. (2011) Randomized trial of the effect of the low molecular weight heparin nadroparin on survival in patients with cancer. J Clin Oncol 29: 2071-6.
22. Gitenay D, Baron VT, (2009) Is Egr1 a potential target for prostate cancer therapy? Future Oncol 5: 993-1003.
23. Recio JA, Merlino G, (2003) Hepatocyte growth factor/scatter factor induces feedback up-regulation of CD44v6 in melanoma cells through Egr-1. Cancer Res 63: 1576-82.
24. Worden B, Yang XP, Lee TL, Bagain L, Yeh NT, et al. (2005) Hepatocyte growth factor/scatter factor differentially regulates expression of proangiogenic factors through Egr-1 in head and neck squamous cell carcinoma. Cancer Res 65: 7071-80.
25. Lee KH, Kim JR, (2009) Hepatocyte growth factor induced up-regulations of VEGF through Egr-1 in hepatocellular carcinoma cells. Clin Exp Metastasis 26: 685-92.
26. Grotegut S, von Schweinitz D, Christofori G, Lehembre F, (2006) Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J 25: 3534-45.
27. Shin SY, Kim JH, Baker A, Lim Y, Lee YH, (2010) Transcription factor Egr-1 is essential for maximal matrix metalloproteinase-9 transcription by tumor necrosis factor alpha. Mol Cancer Res 8: 507-19.
28. Bouchard F, Bélanger SD, Biron-Pain K, St-Pierre Y, (2010) EGR-1 activation by EGF inhibits MMP-9 expression and lymphoma growth. Blood 116: 759-66.
29. Peruzzi B, Bottaro DP, (2006) Targeting the c-Met signaling pathway in cancer. Clin Cancer Res 12: 3657-60.
30. Steffan JJ, Coleman DT, Cardelli JA, (2011) The HGF-met signaling axis: emerging themes and targets of inhibition. Curr Protein Pept Sci 1: 12-22.
31. Wang SW, Pan SL, Peng CY, Huang DY, Tsai AC, et al. (2007) CHM-1 inhibits hepatocyte growth factor-induced invasion of SK-Hep-1 human hepatocellular carcinoma cells by suppressing matrix metalloproteinase-9 expression. Cancer Lett 257: 87-96.
32. Kudo M, (2011) Molecular targeted therapy for hepatocellular carcinoma: bench to bedside. Dig Dis 29: 273-7.
33. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
34. Ogunwobi OO, Liu C, (2011) Hepatocyte growth factor upregulation promotes carcinogenesis and epithelial-mesenchymal transition in hepatocellular carcinoma via Akt and COX-2 pathways. Clin Exp Metastasis 8: 721-31.
35. Akl EA, Labedi N, Terrenato I, Barba M, Sperati F, et al. (2011) Low molecular weight heparin versus unfractionated heparin for perioperative thromboprophylaxis in patients with cancer. Cochrane Database Syst Rev 11: CD009447.
36. Kragh M, Binderup L, Vig Hjarnaa PJ, Bramm E, Johansen KB, et al. (2005) Non-anti-coagulant heparin inhibits metastasis but not primary tumor growth. Oncol Rep 1: 99-104.
37. Ma L, Qiao H, He C, Yang Q, Cheung CHA, et al. (2012) Modulating the interaction of CXCR4 and CXCL12 by low-molecular-weight heparin inhibits hepatic metastasis of colon cancer. Invest New Drugs 22: 508-17.
38. Chalkiadaki G, Nikitovic D, Katonis P, Berdiaki A, Tsatsakis A, et al. (2011) Low molecular weight heparin inhibits melanoma cell adhesion and migration through a PKCa/JNK signaling pathway inducing actin cytoskeleton changes. Cancer Lett 312: 235-44 doi: 10.1016/j.canlet.2011.08.016.
39. Heideman DA, Overmeer RM, van Beusechem VW, Lamers WH, Hakvoort TB, et al. (2005) Inhibition of angiogenesis and HGF-cMET-elicited malignant processes in human hepatocellular carcinoma cells using adenoviral vector-mediated NK4 gene therapy. Cancer Gene Ther 12: 954-62.
40. Ushio K, Hashimoto T, Kitamura N, Tanaka T, (2009) Id1 is down-regulated by hepatocyte growth factor via ERK-dependent and ERK-independent signaling pathways, leading to increased expression of p16INK4a in hepatoma cells. Mol Cancer Res 7: 1179-88.
41. Quinones A, Dobberstein KU, Rainov NG, (2003) The egr-1 gene is induced by DNA-damaging agents and non-genotoxic drugs in both normal and neoplastic human cells. Life Sci 72: 2975-92.
42. Baron V, Adamson ED, Calogero A, Ragona G, Mercola D, (2006) The transcription factor Egr1 is a direct regulator of multiple tumor suppressors including TGFβ1, PTEN, p53, and fibronectin: Egr1 is a potential target of gene therapy for prostate cancer. Cancer Gene Ther 2: 115-124.
43. Virolle T, Adamson ED, Baron V, Birle D, Mercola D, et al. (2001) The Egr-1 transcription factor directly activates PTEN during irradiation-induced signalling. Nat Cell Biol 3: 1124-8.
44. Peng WX, Pan FY, Liu XJ, Ning S, Xu N, et al. (2010) Hypoxia stabilizes microtubule networks and decreases tumor cell chemosensitivity to anticancerdrugs through Egr-1. Anat Rec (Hoboken) 293: 414-20.
45. Krones-Herzig A, Mittal S, Yule K, Liang H, English C, et al. (2005) Early growth response 1 acts as a tumor suppressor in vivo and in vitro via regulation of p53. Cancer Res 65: 5133-43.
46. Levin WJ, Press MF, Gaynor RB, Sukhatme VP, Boone TC, et al. (1995) Expression patterns of immediate early transcription factors in human non-small cell lung cancer. The Lung Cancer Study Group. Oncogene 7: 1261-9.
47. Huang RP, Fan Y, de Belle I, Niemeyer C, Gottardis MM, et al. (1997) Decreased Egr-1 expression in human, mouse and rat mammary cells and tissues correlates with tumor formation. Int J Cancer 72: 102-9.
48. Pignatelli M, Luna-Medina R, Pérez-Rendón A, Santos A, Perez-Castillo A, (2003) The transcription factor early growth response factor-1 (EGR-1) promotes apoptosis of neuroblastoma cells. Biochem J 373: 739-46.
49. Yu J, Zhang SS, Saito K, Williams S, Arimura Y, et al. (2009) PTEN regulation by Akt-Egr1-ARF-PTEN axis. EMBO J 28: 21-33.
50. Dussmann P, Pagel JI, Vogel S, Magnusson T, Zimmermann R, et al. (2011) Live in vivo imaging of Egr-1 promoter activity during neonatal development, liver regeneration and wound healing. BMC Developmental Biology 11: 28.
51. Kawashi{dotless}ta Y, Ohtsuru A, Kaneda Y, Nagaya Y, Kawazoe Y, et al. (1999) Regression of hepatocellular carcinoma in vitro and in vivo by radiosensitizing suicide gene therapy under the inducible and spatial control of radiation. Human Gene Therapy 10: 1509-1519.
52. Hao MW, Liang YR, Liu YF, Liu L, Wu MY, et al. (2002) Transcription factor EGR-1 inhibits growth of hepatocellular carcinoma and esophageal carcinoma cell lines. World J Gastroenterol 2: 203-7.
53. Damm S, Koefinger P, Stefan M, Wels C, Mehes G, et al. (2010) HGF-promoted motility in primary human melanocytes depends on CD44v6 regulated via NF-kappa B, Egr-1, and C/EBP-beta. J Invest Dermatol 30: 1893-903.
54. Ozaki I, Mizuta T, Zhao G, Zhang H, Yoshimura T, et al. (2003) Induction of multiple matrix metalloproteinase genes in human hepatocellular carcinoma by hepatocyte growth factor via a transcription factor Ets-1. Hepatol Res 4: 289-301.
55. Li J, Lau GK, Chen L, Dong SS, Lan HY, et al. (2011) Interleukin 17A promotes hepatocellular carcinoma metastasis via NF-kB induced matrix metalloproteinases 2 and 9 expression. PLoS One 6: e21816.
56. Xu J, Xu HY, Zhang Q, Song F, Jiang JL, et al. (2007) HAb18G/CD147 functions in invasion and metastasis of hepatocellular carcinoma. Mol Cancer Res 6: 605-14.
57. Gaggioli C, Deckert M, Robert G, Abbe P, Batoz M, et al. (2005) HGF induces fibronectin matrix synthesis in melanoma cells through MAP kinase-dependent signaling pathway and induction of Egr-1. Oncogene 24: 1423-1433.
58. Sayan AE, Sayan BS, Findikli N, Ozturk M, (2001) Acquired expression of transcriptionally active p73 in hepatocellular carcinoma cells. Oncogene 20: 5111-5117.
59. Cokakli M, Erdal E, Nart D, Yilmaz F, Sagol O, et al. (2009) Differential expression of Caveolin-1 in hepatocellular carcinoma: correlation with differentiation state, motility and invasion. BMC Cancer 9: 65.
60. Hickok JR, Sahni S, Mikhed Y, Bonini MG, Thomas DD, (2011) Nitric oxide suppresses tumor cell migration through N-Myc downstream-regulated gene-1(NDRG1) expression: role of chelatable iron. J Biol Chem 286: 41413-24.
61. Chen CC, Lee WR, Safe S, (2004) Egr1 is activated by 17beta-estradiol in MCF-7 cells by mitogen-activated protein kinase-dependent phosphorylation of ELK-1. J Cell Biochem 93: 1063-74.