Hepatoprotective and anti-tumor effects of targeting MMP-9 in hepatocellular carcinoma and its relation to vascular invasion markers

Clinical and Experimental Metastasis

Volumn 32, Issue 5, 2015, Pages 479-493

  Elewa, Mohammed A F ^a,b   Al Gayyar, Mohammed M ^b,c   Schaalan, Mona F ^a   Abd El Galil, Khaled H ^d   Ebrahim, Mohamed A ^b   El Shishtawy, Mamdouh M ^b  

^a MISR INTERNATIONAL UNIVERSITY   (Egypt)

^b MANSOURA UNIVERSITY   (Egypt)

^c UNIVERSITY OF TABUK   (Saudi Arabia)

^d MANSOURA UNIVERSITY   (Egypt)

Author keywords

Doxycycline; Fascin; Hepatocellular carcinoma; HSPGs; MMP 9; Oxidative stress

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ALPHA FETOPROTEIN; BILIRUBIN; DOXYCYCLINE HYCLATE; FASCIN; FIBROBLAST GROWTH FACTOR 2; GELATINASE B; GLUTATHIONE; GLUTATHIONE DISULFIDE; MALONALDEHYDE; PROTEOHEPARAN SULFATE; ACTIN BINDING PROTEIN; ANTIINFECTIVE AGENT; ANTIOXIDANT; CARRIER PROTEIN; DOXYCYCLINE; MESSENGER RNA;

ADULT; AGED; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALBUMIN BLOOD LEVEL; ALPHA FETOPROTEIN BLOOD LEVEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BILIRUBIN BLOOD LEVEL; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; IN VIVO STUDY; LIVER; LIVER CELL; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER HOMOGENATE; LIVER LOBULE; LIVER PROTECTION; MAJOR CLINICAL STUDY; MALE; NONHUMAN; OXIDATIVE STRESS; RAT; TUMOR INVASION; VERY ELDERLY; ANIMAL; CANCER STAGING; CARCINOMA, HEPATOCELLULAR; CASE CONTROL STUDY; CHEMISTRY; COMPARATIVE STUDY; ENZYME IMMUNOASSAY; ENZYMOLOGY; FOLLOW UP; GENETICS; LIVER NEOPLASMS; METABOLISM; MIDDLE AGED; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIOXIDANTS; CARCINOMA, HEPATOCELLULAR; CARRIER PROTEINS; CASE-CONTROL STUDIES; DOXYCYCLINE; FEMALE; FIBROBLAST GROWTH FACTOR 2; FOLLOW-UP STUDIES; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; IMMUNOENZYME TECHNIQUES; LIVER NEOPLASMS; MALE; MATRIX METALLOPROTEINASE 9; MICROFILAMENT PROTEINS; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM STAGING; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84930574419     PISSN: 02620898     EISSN: 15737276     Source Type: Journal    
DOI: 10.1007/s10585-015-9721-6     Document Type: Article

References (85)

1. He S et al (2013) Study of RNA interference targeting NET-1 combination with sorafenib for hepatocellular carcinoma therapy in vitro and in vivo. Gastroenterol Res Pract 2013:685150
2. Sun Q et al (2014) Notch1 is a potential therapeutic target for the treatment of human hepatitis B virus X protein-associated hepatocellular carcinoma. Oncol Rep 31(2):933–939
3. Breuhahn K, Schirmacher P (2008) Reactivation of the insulin-like growth factor-II signaling pathway in human hepatocellular carcinoma. World J Gastroenterol 14(11):1690–1698
4. Yao DF, Dong ZZ, Yao M (2007) Specific molecular markers in hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int 6(3):241–247
5. Abdel-Rahman O (2013) Systemic therapy for hepatocellular carcinoma (HCC): from bench to bedside. J Egypt Natl Cancer Inst 25(4):165–171
6. Chen K et al (2014) Rationale of personalized immunosuppressive medication for hepatocellular carcinoma patients after liver transplantation. Liver Transplant Off Publ Am Assoc Study Liver Dis Int Liver Transplant Soc 20(3):261–269
7. Qin LX, Tang ZY (2002) The prognostic molecular markers in hepatocellular carcinoma. World J Gastroenterol 8(3):385–392
8. Jain RK (2003) Molecular regulation of vessel maturation. Nat Med 9(6):685–693
9. Yancopoulos GD et al (2000) Vascular-specific growth factors and blood vessel formation. Nature 407(6801):242–248
10. Lai JP et al (2008) Heparin-degrading sulfatases in hepatocellular carcinoma: roles in pathogenesis and therapy targets. Future Oncol (Lond Engl) 4(6):803–814
11. Segev A, Strauss BH (2004) Novel approaches for the treatment of chronic total coronary occlusions. J Interv Cardiol 17(6):411–416
12. Dong S, Wu XZ (2010) Heparanase and hepatocellular carcinoma: promoter or inhibitor? World J Gastroenterol 16(3):306–311
13. Tsunematsu H et al (2012) Fibroblast growth factor-2 enhances NK sensitivity of hepatocellular carcinoma cells. Int J Cancer 130(2):356–364
14. Ornitz DM et al (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271(25):15292–15297
15. Wang L et al (2012) A novel monoclonal antibody to fibroblast growth factor 2 effectively inhibits growth of hepatocellular carcinoma xenografts. Mol Cancer Ther 11(4):864–872
16. Parks WC, Wilson CL, Lopez-Boado YS (2004) Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 4(8):617–629
17. Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221–233
18. Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2(3):161–174
19. Kessenbrock K, Plaks V, Werb Z (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141(1):52–67
20. Kim KR et al (2011) The role of serum response factor in hepatocellular carcinoma: an association with matrix metalloproteinase. Oncol Rep 26(6):1567–1572
21. Deryugina EI, Quigley JP (2006) Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 25(1):9–34
22. Hidalgo M, Eckhardt SG (2001) Development of matrix metalloproteinase inhibitors in cancer therapy. J Natl Cancer Inst 93(3):178–193
23. Tae HJ et al (2012) Chronic treatment with a broad-spectrum metalloproteinase inhibitor, doxycycline, prevents the development of spontaneous aortic lesions in a mouse model of vascular Ehlers–Danlos syndrome. J Pharmacol Exp Ther 343(1):246–251
24. Nowak E et al (2013) MMP-9 directed shRNAs as relevant inhibitors of matrix metalloproteinase 9 activity and signaling. Postepy Hig Med Dosw (Online) 67:742–749
25. Shuman Moss LA, Jensen-Taubman S, Stetler-Stevenson WG (2012) Matrix metalloproteinases: changing roles in tumor progression and metastasis. Am J Pathol 181(6):1895–1899
26. Yamashiro S, et al. (1998) Fascin, an actin-bundling protein, induces membrane protrusions and increases cell motility of epithelial cells. Molecular biology of the cell 9 5: 993-1006
27. Jayo A, Parsons M (2010) Fascin: a key regulator of cytoskeletal dynamics. Int J Biochem Cell Biol 42(10):1614–1617
28. Huang X et al (2012) Fascin and cortactin expression is correlated with a poor prognosis in hepatocellular carcinoma. Eur J Gastroenterol Hepatol 24(6):633–639
29. Young IS, Woodside JV (2001) Antioxidants in health and disease. J Clin Pathol 54(3):176–186
30. Cross CE et al (1998) Oxidative stress and antioxidants at biosurfaces: plants, skin, and respiratory tract surfaces. Environ Health Perspect 106(Suppl 5):1241–1251
31. Tayel A et al (2014) Suramin inhibits hepatic tissue damage in hepatocellular carcinoma through deactivation of heparanase enzyme. Eur J Pharmacol 728:151–160
32. Darweish MM et al (2014) Chemopreventive and hepatoprotective effects of Epigallocatechin-gallate against hepatocellular carcinoma: role of heparan sulfate proteoglycans pathway. J Pharm Pharmacol 66(7):1032–1045
33. Zaghloul RA et al (2015) Evaluation of antiglypican-3 therapy as a promising target for amelioration of hepatic tissue damage in hepatocellular carcinoma. Eur J Pharmacol 746:353–362
34. Brookes ZL, Reilly CS, Brown NJ (2004) Differential effects of propofol, ketamine, and thiopental anaesthesia on the skeletal muscle microcirculation of normotensive and hypertensive rats in vivo. Br J Anaesth 93(2):249–256
35. Brookes ZL et al (2007) Proinflammatory and vasodilator effects of nociceptin/orphanin FQ in the rat mesenteric microcirculation are mediated by histamine. Am J Physiol Heart Circ Physiol 293(5):H2977–H2985
36. Draper HH, McGirr LG, Hadley M (1986) The metabolism of malondialdehyde. Lipids 21(4):305–307
37. Eyer P, Podhradsky D (1986) Evaluation of the micromethod for determination of glutathione using enzymatic cycling and Ellman’s reagent. Anal Biochem 153(1):57–66
38. Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem/FEBS 47(3):469–474
39. Cohen G, Dembiec D, Marcus J (1970) Measurement of catalase activity in tissue extracts. Anal Biochem 34:30–38
40. Hadler-Olsen E, Winberg JO, Uhlin-Hansen L (2013) Matrix metalloproteinases in cancer: their value as diagnostic and prognostic markers and therapeutic targets. Tumour Biol J Int Soc Oncodev Biol Med 34(4):2041–2051
41. Toyoshima M, Nakajima M (1999) Human heparanase. Purification, characterization, cloning, and expression. J Biol Chem 274(34):24153–24160
42. Ornitz DM (2000) FGFs, heparan sulfate and FGFRs: complex interactions essential for development. BioEssays News Reviews Mol Cell Dev Biol 22(2):108–112
43. Harmer NJ (2006) Insights into the role of heparan sulphate in fibroblast growth factor signalling. Biochem Soc Trans 34(Pt 3):442–445
44. Powell WC, Matrisian LM (1996) Complex roles of matrix metalloproteinases in tumor progression. Curr Top Microbiol Immunol 213(Pt 1):1–21
45. Goncalves JL et al (2012) Pro-inflammatory effects of the mushroom Agaricus blazei and its consequences on atherosclerosis development. Eur J Nutr 51(8):927–937
46. Ordonez R et al (2014) Inhibition of matrix metalloproteinase-9 and nuclear factor kappa B contribute to melatonin prevention of motility and invasiveness in HepG2 liver cancer cells. J Pineal Res 56(1):20–30
47. Lou L et al (2013) Enhancement of invasion of hepatocellular carcinoma cells through lysophosphatidic acid receptor. J Int Med Res 41(1):55–63
48. Roomi MW et al (2013) In vitro modulation of MMP-2 and MMP-9 in adult human sarcoma cell lines by cytokines, inducers and inhibitors. Int J Oncol 43(6):1787–1798
49. Carey DJ (1997) Syndecans: multifunctional cell-surface co-receptors. Biochem J 327(Pt 1):1–16
50. Bernfield M et al (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729–777
51. Purushothaman A et al (2008) Heparanase stimulation of protease expression implicates it as a master regulator of the aggressive tumor phenotype in myeloma. J Biol Chem 283(47):32628–32636
52. Chen L, Sanderson RD (2009) Heparanase regulates levels of syndecan-1 in the nucleus. PloS One 4(3):e4947
53. Yang Y et al (2002) Soluble syndecan-1 promotes growth of myeloma tumors in vivo. Blood 100(2):610–617
54. Li Q et al (2002) Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111(5):635–646
55. Yang X et al (2009) Signal transducers and activators of transcription mediate fibroblast growth factor-induced vascular endothelial morphogenesis. Cancer Res 69(4):1668–1677
56. Sharma B et al (1998) Antisense targeting of perlecan blocks tumor growth and angiogenesis in vivo. J Clin Investig 102(8):1599–1608
57. Kanazawa S et al (2001) VEGF, basic-FGF, and TGF-beta in Crohn’s disease and ulcerative colitis: a novel mechanism of chronic intestinal inflammation. Am J Gastroenterol 96(3):822–828
58. Tassi E et al (2011) Impact of fibroblast growth factor-binding protein-1 expression on angiogenesis and wound healing. Am J Pathol 179(5):2220–2232
59. Lin ZY, Chuang WL (2013) Hepatocellular carcinoma cells cause different responses in expressions of cancer-promoting genes in different cancer-associated fibroblasts. Kaohsiung J Med Sci 29(6):312–318
60. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112(4):453–465
61. Hashimoto Y et al (2006) Prognostic significance of fascin expression in advanced colorectal cancer: an immunohistochemical study of colorectal adenomas and adenocarcinomas. BMC Cancer 6:241
62. Vignjevic D et al (2007) Fascin, a novel target of beta-catenin-TCF signaling, is expressed at the invasive front of human colon cancer. Cancer Res 67(14):6844–6853
63. Hayashi Y, Osanai M, Lee GH (2011) Fascin-1 expression correlates with repression of E-cadherin expression in hepatocellular carcinoma cells and augments their invasiveness in combination with matrix metalloproteinases. Cancer Sci 102(6):1228–1235
64. Lee TK et al (2007) Fascin over-expression is associated with aggressiveness of oral squamous cell carcinoma. Cancer Lett 254(2):308–315
65. Zhao Q et al (2010) Phosphorylation of fascin decreases the risk of poor survival in patients with esophageal squamous cell carcinoma. J Histochem Cytochem Off J Histochem Soc 58(11):979–988
66. Oh SY et al (2012) Prognostic impact of fascin-1 expression is more significant in advanced colorectal cancer. J Surg Res 172(1):102–108
67. Griffin MO et al (2010) Tetracyclines: a pleiotropic family of compounds with promising therapeutic properties. Review of the literature. Am J Physiol Cell Physiol 299(3):C539–C548
68. Peterson JT (2004) Matrix metalloproteinase inhibitor development and the remodeling of drug discovery. Heart Fail Rev 9(1):63–79
69. Seftor RE et al (1998) Chemically modified tetracyclines inhibit human melanoma cell invasion and metastasis. Clin Exp Metastasis 16(3):217–225
70. Lokeshwar BL et al (2002) Inhibition of cell proliferation, invasion, tumor growth and metastasis by an oral non-antimicrobial tetracycline analog (COL-3) in a metastatic prostate cancer model. Int J Cancer 98(2):297–309
71. Ryan ME, et al. (2001) Excessive matrix metalloproteinase activity in diabetes: inhibition by tetracycline analogues with zinc reactivity. Current medicinal chemistry 8 3: 305-16
72. Roomi MW et al (2014) In vitro modulation of MMP-2 and MMP-9 in pediatric human sarcoma cell lines by cytokines, inducers and inhibitors. Int J Oncol 44(1):27–34
73. Sun B et al (2007) Doxycycline influences microcirculation patterns in B16 melanoma. Exp Biol Med (Maywood, NJ) 232(10):1300–1307
74. Krylova IV, Shalaev VA, Isakov SV (1991) Individual prognosis of chronic B-lymphoid leukemia course. Gematol transfuziol 36(10):19–21
75. Wang CY et al (2013) Activation of PPARgamma is required for hydroxysafflor yellow A of Carthamus tinctorius to attenuate hepatic fibrosis induced by oxidative stress. Phytomed Int J Phytother Phytopharmacol 20(7):592–599
76. Calvisi DF et al (2005) Activation of the canonical Wnt/beta-catenin pathway confers growth advantages in c-Myc/E2F1 transgenic mouse model of liver cancer. J Hepatol 42(6):842–849
77. Li T et al (2013) Glutathione S-transferase P1 correlated with oxidative stress in hepatocellular carcinoma. Int J Med Sci 10(6):683–690
78. Weiss SJ et al (1985) Oxidative autoactivation of latent collagenase by human neutrophils. Science (New York, NY) 227(4688):747–749
79. Senturker S et al (1997) Oxidative DNA base damage and antioxidant enzyme levels in childhood acute lymphoblastic leukemia. FEBS Lett 416(3):286–290
80. Liu DY et al (2003) Expression of telomerase activity and oxidative stress in human hepatocellular carcinoma with cirrhosis. World J Gastroenterol 9(8):1859–1862
81. Yagan A, Kesim S, Liman N (2014) Effect of low-dose doxycycline on serum oxidative status, gingival antioxidant levels, and alveolar bone loss in experimental periodontitis in rats. J Periodontol 85(3):478–489
82. Creemers EE et al (2001) Matrix metalloproteinase inhibition after myocardial infarction: a new approach to prevent heart failure? Circ Res 89(3):201–210
83. Park JL, Lucchesi BR (1999) Mechanisms of myocardial reperfusion injury. Ann Thorac Surg 68(5):1905–1912
84. Kraus RL et al (2005) Antioxidant properties of minocycline: neuroprotection in an oxidative stress assay and direct radical-scavenging activity. J Neurochem 94(3):819–827
85. Hashimoto Y, Parsons M, Adams JC (2007) Dual actin-bundling and protein kinase C-binding activities of fascin regulate carcinoma cell migration downstream of Rac and contribute to metastasis. Mol Biol Cell 18(11):4591–4602