Suramin inhibits hepatic tissue damage in hepatocellular carcinoma through deactivation of heparanase enzyme

European Journal of Pharmacology

Volumn 728, Issue 1, 2014, Pages 151-160

  Tayel, Ahmed ^a   Abd El Galil, Khaled H ^b   Ebrahim, Mohamed A ^c   Ibrahim, Ahmed S ^a   El Gayar, Amal M ^a   Al Gayyar, Mohammed M H ^a  

^a MANSOURA UNIVERSITY   (Egypt)

^b University of Mansoura   (Egypt)

^c MANSOURA UNIVERSITY   (Egypt)

Author keywords

Extrinsic cell death; Fibroblast Growth Factor (FGF) 2; Glucosamine; Glucuronic acid; Heparan sulfate proteoglycans (HSPGs); Intrinsic cell death

Indexed keywords

ALPHA FETOPROTEIN; CASPASE 3; CASPASE 8; CASPASE 9; FIBROBLAST GROWTH FACTOR 2; GLUCOSAMINE; GLUCURONIC ACID; HEPARANASE; PROTEOHEPARAN SULFATE; SURAMIN; ANTINEOPLASTIC AGENT; BETA GLUCURONIDASE;

ADULT; AGED; ALPHA FETOPROTEIN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CHEMOPROPHYLAXIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; HUMAN; IN VIVO STUDY; LIVER CELL CARCINOMA; LIVER FIBROSIS; LIVER INJURY; LIVER PROTECTION; MAJOR CLINICAL STUDY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOMA, HEPATOCELLULAR; CHEMICALLY INDUCED; DRUG EFFECTS; ENZYMOLOGY; GENETICS; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; METABOLISM; MIDDLE AGED; OXIDATIVE STRESS; PATHOLOGY; SPRAGUE DAWLEY RAT; SURVIVAL;

ADULT; ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, HEPATOCELLULAR; FEMALE; GLUCURONIDASE; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MIDDLE AGED; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SURAMIN; SURVIVAL ANALYSIS;

EID: 84896712475     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2014.02.001     Document Type: Article

References (58)

1. M.M. Al-Gayyar, M.A. Ebrahim, and M.E. Shams Measuring serum levels of glycosaminoglycans for prediction and using viscum fraxini-2 for treatment of patients with hepatocellular carcinoma J. Pharm. Res. 7 2013 571 575
2. M.A. Avila, C. Berasain, B. Sangro, and J. Prieto New therapies for hepatocellular carcinoma Oncogene 25 2006 3866 3884 (Pubitemid 43980482)
3. T. Ben Moshe, H. Barash, T.B. Kang, J.C. Kim, A. Kovalenko, E. Gross, M. Schuchmann, R. Abramovitch, E. Galun, and D. Wallach Role of caspase-8 in hepatocyte response to infection and injury in mice Hepatology 45 2007 1014 1024 (Pubitemid 46631570)
4. A.L. Cheng, Y.C. Shen, and A.X. Zhu Targeting fibroblast growth factor receptor signaling in hepatocellular carcinoma Oncology 81 2011 372 380
5. L.N. Cruz, M.A. Juliano, A. Budu, L. Juliano, A.A. Holder, M.J. Blackman, and C.R. Garcia Extracellular ATP triggers proteolysis and cytosolic Ca(2)(+) rise in Plasmodium berghei and Plasmodium yoelii malaria parasites Malar. J. 11 2012 69
6. N.A. Dawson, R.M. Lush, S.M. Steinberg, A.C. Tompkins, D.J. Headlee, and W.D. Figg Suramin-induced neutropenia Eur. J. Cancer 32A 1996 1534 1539 (Pubitemid 26279120)
7. L.R. DeChatelet, C.E. McCall, L.C. McPhail, and R.B. Johnston Jr. Superoxide dismutase activity in leukocytes J. Clin. Invest. 53 1974 1197 1201
8. H.H. Draper, and M. Hadley A review of recent studies on the metabolism of exogenous and endogenous malondialdehyde Xenobiotica 20 1990 901 907 (Pubitemid 20294520)
9. L.A. Elson, and W.T. Morgan A colorimetric method for the determination of glucosamine and chondrosamine Biochem. J. 27 1933 1824 1828
10. B. Fang, G. Fu, J. Agniswamy, R.W. Harrison, and I.T. Weber Caspase-3 binds diverse P4 residues in peptides as revealed by crystallography and structural modeling Apoptosis 14 2009 741 752
11. V. Ferro, E. Hammond, and J.K. Fairweather The development of inhibitors of heparanase, a key enzyme involved in tumour metastasis, angiogenesis and inflammation Mini. Rev. Med. Chem. 4 2004 693 702 (Pubitemid 38961234)
12. R. Flaumenhaft, D. Moscatelli, and D.B. Rifkin Heparin and heparan sulfate increase the radius of diffusion and action of basic fibroblast growth factor J. Cell Biol. 111 1990 1651 1659
13. S. Fulda, and K.M. Debatin Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy Oncogene 25 2006 4798 4811 (Pubitemid 44187627)
14. L. Fux, N. Ilan, R.D. Sanderson, and I. Vlodavsky Heparanase: busy at the cell surface Trends Biochem. Sci. 34 2009 511 519
15. J.A. Garson, D. Lubach, J. Passas, K. Whitby, and P.R. Grant Suramin blocks hepatitis C binding to human hepatoma cells in vitro J. Med. Virol. 57 1999 238 242 (Pubitemid 29069730)
16. A.I. Gomaa, S.A. Khan, M.B. Toledano, I. Waked, and S.D. Taylor-Robinson Hepatocellular carcinoma: epidemiology, risk factors and pathogenesis World J. Gastroenterol. 14 2008 4300 4308
17. S. He, H. Rehman, Y. Shi, Y. Krishnasamy, J.J. Lemasters, R.G. Schnellmann, and Z. Zhong Suramin decreases injury and improves regeneration of ethanol-induced steatotic partial liver grafts J. Pharmacol. Exp. Ther. 344 2013 417 425
18. M. Ho Advances in liver cancer antibody therapies: a focus on glypican-3 and mesothelin BioDrugs 25 2011 275 284
19. H.W. Huang, S.K. Mohan, and C. Yu The NMR solution structure of human epidermal growth factor (hEGF) at physiological pH and its interactions with suramin Biochem. Biophys. Res. Commun. 402 2010 705 710
20. N. Ilan, M. Elkin, and I. Vlodavsky Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis Int. J. Biochem. Cell Biol. 38 2006 2018 2039 (Pubitemid 44397619)
21. X. Li, I.S. Benjamin, and B. Alexander Reproducible production of thioacetamide-induced macronodular cirrhosis in the rat with no mortality J. Hepatol. 36 2002 488 493 (Pubitemid 34407336)
22. R.R. Liang, S. Zhang, J.A. Qi, Z.D. Wang, J. Li, P.J. Liu, C. Huang, X.F. Le, J. Yang, and Z.F. Li Preferential inhibition of hepatocellular carcinoma by the flavonoid Baicalein through blocking MEK-ERK signaling Int. J. Oncol. 41 2012 969 978
23. C. Liedtke, J.M. Bangen, J. Freimuth, N. Beraza, D. Lambertz, F.J. Cubero, M. Hatting, K.R. Karlmark, K.L. Streetz, G.A. Krombach, F. Tacke, N. Gassler, D. Riethmacher, and C. Trautwein Loss of caspase-8 protects mice against inflammation-related hepatocarcinogenesis but induces non-apoptotic liver injury Gastroenterology 141 2011 2176 2187
24. X. Lin, E.M. Buff, N. Perrimon, and A.M. Michelson Heparan sulfate proteoglycans are essential for FGF receptor signaling during Drosophila embryonic development Development 126 1999 3715 3723 (Pubitemid 29440471)
25. N. Liu, and S. Zhuang Tissue protective and anti-fibrotic actions of suramin: new uses of an old drug Curr. Clin. Pharmacol. 6 2011 137 142
26. M.H. Lowitt, M. Eisenberger, B. Sina, and G.F. Kao Cutaneous eruptions from suramin. A clinical and histopathologic study of 60 patients Arch. Dermatol. 131 1995 1147 1153
27. D. Marchetti, J. Reiland, B. Erwin, and M. Roy Inhibition of heparanase activity and heparanase-induced angiogenesis by suramin analogues Int. J. Cancer 104 2003 167 174 (Pubitemid 36249791)
28. E.A. McKenzie Heparanase: a target for drug discovery in cancer and inflammation Br. J. Pharmacol. 151 2007 1 14 (Pubitemid 46675998)
29. R.E. Mosher Interferences in the colorimetric determination of glucuronic acid in blood serum Clin. Chem. 8 1962 378 388
30. M. Nakajima, A. DeChavigny, C.E. Johnson, J. Hamada, C.A. Stein, and G.L. Nicolson Suramin. A potent inhibitor of melanoma heparanase and invasion J. Biol. Chem. 266 1991 9661 9666 (Pubitemid 21906707)
31. P. Newell, A. Villanueva, S.L. Friedman, K. Koike, and J.M. Llovet Experimental models of hepatocellular carcinoma J. Hepatol. 48 2008 858 879
32. P.W. Noble Hyaluronan and its catabolic products in tissue injury and repair Matrix Biol. 21 2002 25 29 (Pubitemid 34100819)
33. M. Okabe, M. Enomoto, H. Maeda, K. Kuroki, and K. Ohtsuki Biochemical characterization of suramin as a selective inhibitor for the PKA-mediated phosphorylation of HBV core protein in vitro Biol. Pharm. Bull. 29 2006 1810 1814 (Pubitemid 44338399)
34. D.M. Ornitz FGFs, heparan sulfate and FGFRs: complex interactions essential for development Bioessays 22 2000 108 112 (Pubitemid 30092077)
35. C.R. Parish, C. Freeman, and M.D. Hulett Heparanase: a key enzyme involved in cell invasion Biochim. Biophys. Acta 1471 2001 M99 M108
36. R. Persad, C. Liu, T.T. Wu, P.S. Houlihan, S.R. Hamilton, A.M. Diehl, and A. Rashid Overexpression of caspase-3 in hepatocellular carcinomas Mod. Pathol. 17 2004 861 867
37. E. Pesenti, F. Sola, N. Mongelli, M. Grandi, and F. Spreafico Suramin prevents neovascularisation and tumour growth through blocking of basic fibroblast growth factor activity Br. J. Cancer 66 1992 367 372
38. J.C. Reed Mechanisms of apoptosis Am. J. Pathol. 157 2000 1415 1430
39. M.P. Ricciardi, P. Soldani, A. Paparelli, M. Gesi, and A. Pellegrini Morphohistochemical relationships between adrenal cortex and major salivary glands in response to chronic suramin treatment Acta Histochem. 97 1995 151 158
40. P.R. Romano, D.E. McCallus, and C.J. Pachuk RNA interference-mediated prevention and therapy for hepatocellular carcinoma Oncogene 25 2006 3857 3865 (Pubitemid 43980481)
41. M. Sakamoto, T. Mori, Y. Masugi, K. Effendi, I. Rie, and W. Du Candidate molecular markers for histological diagnosis of early hepatocellular carcinoma Intervirology 51 suppl 1 2008 42 45 (Pubitemid 351821841)
42. R.D. Sanderson, Y. Yang, T. Kelly, V. MacLeod, Y. Dai, and A. Theus Enzymatic remodeling of heparan sulfate proteoglycans within the tumor microenvironment: growth regulation and the prospect of new cancer therapies J. Cell Biochem. 96 2005 897 905 (Pubitemid 41688716)
43. R. Sasisekharan, Z. Shriver, G. Venkataraman, and U. Narayanasami Roles of heparan-sulphate glycosaminoglycans in cancer Nat. Rev. Cancer 2 2002 521 528 (Pubitemid 37328933)
44. J.M. Schattenberg, M. Nagel, Y.O. Kim, T. Kohl, M.A. Worns, T. Zimmermann, A. Schad, T. Longerich, D. Schuppan, Y.W. He, P.R. Galle, and M. Schuchmann Increased hepatic fibrosis and JNK2-dependent liver injury in mice exhibiting hepatocyte-specific deletion of cFLIP Am. J. Physiol. Gastrointest Liver Physiol. 303 2012 G498 G506
45. H.I. Scher, D.I. Jodrell, J.M. Iversen, T. Curley, W. Tong, M.J. Egorin, and A. Forrest Use of adaptive control with feedback to individualize suramin dosing Cancer Res. 52 1992 64 70
46. C. Spaniel, M. Honda, S.R. Selitsky, D. Yamane, T. Shimakami, S. Kaneko, R.E. Lanford, and S.M. Lemon microRNA-122 abundance in hepatocellular carcinoma and non-tumor liver tissue from Japanese patients with persistent HCV versus HBV infection PLoS One 8 2013 e76867
47. A. Subramaniam, M.K. Shanmugam, T.H. Ong, F. Li, E. Perumal, L. Chen, S. Vali, T. Abbasi, S. Kapoor, K.S. Ahn, A.P. Kumar, K.M. Hui, and G. Sethi Emodin inhibits growth and induces apoptosis in an orthotopic hepatocellular carcinoma model by blocking activation of STAT3 Br. J. Pharmacol. 170 2013 807 821
48. I. Vlodavsky, M. Elkin, O. Pappo, H. Aingorn, R. Atzmon, R. Ishai-Michaeli, A. Aviv, I. Pecker, and Y. Friedmann Mammalian heparanase as mediator of tumor metastasis and angiogenesis Isr. Med. Assoc. J. 2 Suppl 2000 37 45 (Pubitemid 30614260)
49. I. Vlodavsky, and Y. Friedmann Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis J. Clin. Invest. 108 2001 341 347 (Pubitemid 32730777)
50. I. Vlodavsky, and O. Goldshmidt Properties and function of heparanase in cancer metastasis and angiogenesis Haemostasis 31 Suppl 1 2001 60 63
51. I. Vlodavsky, O. Goldshmidt, E. Zcharia, R. Atzmon, Z. Rangini-Guatta, M. Elkin, T. Peretz, and Y. Friedmann Mammalian heparanase: involvement in cancer metastasis, angiogenesis and normal development Semin. Cancer Biol. 12 2002 121 129 (Pubitemid 34680741)
52. I. Vlodavsky, N. Ilan, A. Naggi, and B. Casu Heparanase: structure, biological functions, and inhibition by heparin-derived mimetics of heparan sulfate Curr. Pharm. Des. 13 2007 2057 2073 (Pubitemid 47044735)
53. V. Vreys, and G. David Mammalian heparanase: what is the message? J. Cell Mol. Med. 11 2007 427 452 (Pubitemid 47153456)
54. S.H. Wang, L.M. Chen, W.K. Yang, and J.D. Lee Increased extrinsic apoptotic pathway activity in patients with hepatocellular carcinoma following transarterial embolization World J. Gastroenterol. 17 2011 4675 4681
55. X.Z. Wu, D. Chen, and G.R. Xie Extracellular matrix remodeling in hepatocellular carcinoma: effects of soil on seed? Med. Hypotheses 66 2006 1115 1120
56. T. Yoshino, H. Tabunoki, S. Sugiyama, K. Ishii, S.U. Kim, and J. Satoh Non-phosphorylated FTY720 induces apoptosis of human microglia by activating SREBP2 Cell Mol. Neurobiol. 31 2011 1009 1020
57. L. Zhang, W.S. Liu, B.Q. Han, Y.F. Peng, and D.F. Wang Antitumor activities of d-glucosamine and its derivatives J. Zhejiang Univ. Sci. B 7 2006 608 614
58. Z. Zhang, C. Zhang, Y. Ding, Q. Zhao, L. Yang, J. Ling, L. Liu, H. Ji, and Y. Zhang The activation of p38 and JNK by ROS, contribute to OLO-2-mediated intrinsic apoptosis in human hepatocellular carcinoma cells Food Chem. Toxicol. 63 2014 38 47