4-Methylumbelliferone inhibits hepatocellular carcinoma growth by decreasing IL-6 production and angiogenesis

Glycobiology

Volumn 25, Issue 8, 2015, Pages 825-835

  Piccioni, Flavia ^a   Fiore, Esteban ^a   Bayo, Juan ^b   Atorrasagasti, Catalina ^a,d   Peixoto, Estanislao ^d   Rizzo, Manglio ^a   Malvicini, Mariana ^a,d   Tirado González, Irene ^b   García, Mariana G ^a,d   Alaniz, Laura ^c,d   Mazzolini, Guillermo ^a,d  

^a UNIVERSIDAD AUSTRAL   (Argentina)

^b HUMBOLDT UNIVERSITY   (Germany)

^c Universidad Nacional del Noroeste de la Provincia de Buenos Aires   (Argentina)

^d CONICET ^*  (Argentina)

Author keywords

4 methylumbelliferone; Angiogenesis; HCC; Hyaluronic acid; IL 6; Liver fibrosis; VEGF

Indexed keywords

CD31 ANTIGEN; HYMECROMONE; INTERLEUKIN 6; MESSENGER RNA; STROMAL CELL DERIVED FACTOR 1; THIOACETAMIDE; VASCULOTROPIN; ANTINEOPLASTIC AGENT; CXCL12 PROTEIN, MOUSE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; KUPFFER CELL; LIVER CELL CARCINOMA; LIVER PARENCHYMA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; THIOACETAMIDE-INDUCED LIVER FIBROSIS; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; C3H MOUSE; CARCINOMA, HEPATOCELLULAR; CELL MOTION; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LIVER CIRRHOSIS; LIVER NEOPLASMS; METABOLISM; MORTALITY; NEOVASCULARIZATION, PATHOLOGIC; ORAL DRUG ADMINISTRATION; PATHOLOGY; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TUMOR CELL LINE;

ADMINISTRATION, ORAL; ANIMALS; ANTIGENS, CD31; ANTINEOPLASTIC AGENTS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL12; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HYMECROMONE; INTERLEUKIN-6; KUPFFER CELLS; LIVER CIRRHOSIS; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED C3H; NEOVASCULARIZATION, PATHOLOGIC; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; THIOACETAMIDE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84940650114     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwv023     Document Type: Article

References (78)

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31. Savani RC, Cao G, Pooler PM, Zaman A, Zhou Z, DeLisser HM. 2001. Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. J Biol Chem. 276(39):36770-36778.
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33. Takeda S, Aburada M. 1981. The choleretic mechanism of coumarin compounds and phenolic compounds. J Pharmacobio-Dyn. 4(9):724-734.
34. Toole BP 2004. Hyaluronan: From extracellular glue to pericellular cue. Nat Rev Cancer. 4(7):528-539.
35. Toole BP 2002. Hyaluronan promotes the malignant phenotype. Glycobiology. 12(3):37R-42R.
36. Vincent T, Jourdan M, Sy M-S, Klein B, Mechti N. 2001. Hyaluronic acid induces survival and proliferation of human myeloma cells through an interleukin-6-mediated pathway involving the phosphorylation of retinoblastoma protein. J Biol Chem. 276(18):14728-14736.
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38. Yoshihara S, Kon A, Kudo D, Nakazawa H, Kakizaki I, Sasaki M, Endo M, Takagaki K. 2005. A hyaluronan synthase suppressor, 4-methylumbelliferone, inhibits liver metastasis of melanoma cells. FEBS Lett. 579(12):2722-2726.
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40. Atorrasagasti C, Peixoto E, Aquino JB, Kippes N, Malvicini M, Alaniz L, Garcia M, Piccioni F, Fiore EJ, Bayo J. 2013. Lack of the matricellular protein SPARC (secreted protein, acidic and rich in cysteine) attenuates liver fibrogenesis in mice. PLoS ONE. 8(2): e54962.
41. Bataller R, Brenner DA. 2005. Liver fibrosis. J Clin Invest. 115(2):209-218.
42. Bissell MJ, Radisky D. 2001. Putting tumours in context. Nat Rev Cancer. 1 (1):46-54.
43. Boregowda RK, Appaiah HN, Siddaiah M, Kumarswamy SB, Sunila S, Thimmaiah K, Mortha K, Toole B, Banerjee Sd. 2006. Expression of hyaluronan in human tumor progression. J Carcinog. 5(1):2.
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45. Carmeliet P, Jain RK. 2011. Molecular mechanisms and clinical applications of angiogenesis. Nature. 473(7347):298-307.
46. Cordo-Russo R, Garcia M, Barrientos G, Orsal A, Viola M, Moschansky P, Ringel F, Passi L, Alaniz L, Hajos S. 2009. Murine abortion is associated with enhanced hyaluronan expression and abnormal localization at the fetomaternal interface. Placenta. 30(1):88-95.
47. Corpechot C, Barbu V, Wendum D, Kinnman N, Rey C, Poupon R, Housset C, Rosmorduc O. 2002. Hypoxia-induced VEGF and collagen I expressions are associated with angiogenesis and fibrogenesis in experimental cirrhosis. Hepatology. 35(5):1010-1021.
48. Coulon S, Heindryckx F, Geerts A, Van Steenkiste C, Colle I, Van Vlierberghe H. 2011. Angiogenesis in chronic liver disease and its complications. Liver Int. 31(2):146-162.
49. Esko JD, Kimata K, Lindahl U. 2009. Proteoglycans and sulfated glycosaminoglycans. 2nd ed. New York (NY): Cold Spring Harbor Laboratory Press.
50. García-Vilas JA, Quesada AR, Medina MAn 2013. 4-Methylumbelliferone inhibits angiogenesis in vitro and in vivo. J Agric Food Chem. 61 (17):4063-4071.
51. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Yung S, Chimenti S, Landsman L, Abramovitch R, Keshet E. 2006. VEGF-induced adult neovascularization: Recruitment, retention, and role of accessory cells. Cell. 124 (1):175-189.
52. Hammerich L, Tacke F. 2014. Interleukins in chronic liver disease: Lessons learned from experimental mouse models. Clin Exp Gastroenterol. 7: 297.
53. He G, Karin M. 2010. NF-κB and STAT3 - key players in liver inflammation and cancer. Cell Res. 21(1):159-168.
54. Hernandez-Gea V, Toffanin S, Friedman SL, Llovet JM. 2013. Role of the microenvironment in the pathogenesis and treatment of hepatocellular carcinoma. Gastroenterology. 144(3):512-527.
55. Hoshida Y, Villanueva A, Kobayashi M, Peix J, Chiang DY, Camargo A, Gupta S, Moore J, Wrobel MJ, Lerner J. 2008. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. New Engl J Med. 359 (19):1995-2004.
56. Itano N, Zhuo L, Kimata K. 2008. Impact of the hyaluronan-rich tumor microenvironment on cancer initiation and progression. Cancer Sci. 99(9): 1720-1725.
57. Jiang D, Liang J, Noble PW. 2011. Hyaluronan as an immune regulator in human diseases. Physiol Rev. 91(1):221-264.
58. Kalluri R. 2003. Basement membranes: Structure, assembly and role in tumour angiogenesis. Nat Rev Cancer. 3(6):422-433.
59. Kojima J, Nakamura N, Kanatani M, Omori K. 1975. The glycosaminoglycans in human hepatic cancer. Cancer Res. 35(3):542-547.
60. Kultti A, Pasonen-Seppänen S, Jauhiainen M, Rilla KJ, Kärnä R, Pyöriä E, Tammi RH, Tammi MI. 2009. 4-Methylumbelliferone inhibits hyaluronan synthesis by depletion of cellular UDP-glucuronic acid and downregulation of hyaluronan synthase 2 and 3. Exp Cell Res. 315(11):1914-1923.
61. Lokeshwar VB, Lopez LE, Munoz D, Chi A, Shirodkar SP, Lokeshwar SD, Escudero DO, Dhir N, Altman N. 2010. Antitumor activity of hyaluronic acid synthesis inhibitor 4-methylumbelliferone in prostate cancer cells. Cancer Res. 70(7):2613-2623.
62. Mummery RS, Rider CC. 2000. Characterization of the heparin-binding properties of IL-6. J Immunol. 165(10):5671-5679.
63. Nagasaki T, Hara M, Nakanishi H, Takahashi H, Sato M, Takeyama H. 2013. Interleukin-6 released by colon cancer-associated fibroblasts is critical for tumour angiogenesis: Anti-interleukin-6 receptor antibody suppressed angiogenesis and inhibited tumour-stroma interaction. Br J Cancer. 110 (2):469-478.
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65. Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, Karin M. 2007. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science. 317(5834):121-124.
66. Noble PW, Lake F, Henson P, Riches D. 1993. Hyaluronate activation of CD44 induces insulin-like growth factor-1 expression by a tumor necrosis factor-alpha-dependent mechanism in murine macrophages. J Clin Invest. 91(6):2368.
67. Piccioni F, Malvicini M, Garcia MG, Rodriguez A, Atorrasagasti C, Kippes N, Buena ITP, Rizzo MM, Bayo J, Aquino J. 2012. Antitumor effects of hyaluronic acid inhibitor 4-methylumbelliferone in an orthotopic hepatocellular carcinoma model in mice. Glycobiology. 22(3):400-410.
68. Ramsden L, Rider CC. 1992. Selective and differential binding of interleukin (IL)-1α, IL-1β, IL-2 and IL-6 to glycosaminoglycans. Eur J Immunol. 22 (11):3027-3031.
69. Rappaport A, MacPhee P, Fisher M, Phillips M. 1983. The scarring of the liver acini (cirrhosis). Virchows Archiv A. 402(2):107-137.
70. Savani RC, Cao G, Pooler PM, Zaman A, Zhou Z, DeLisser HM. 2001. Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. J Biol Chem. 276(39):36770-36778.
71. Hansen B, Arteta B, Smedsrød B. 2002. The physiological scavenger receptor function of hepatic sinusoidal endothelial and Kupffer cells is independent of scavenger receptor class A type I and II. Mol Cell Biochem. 240: 1-8.
72. Takeda S, Aburada M. 1981. The choleretic mechanism of coumarin compounds and phenolic compounds. J Pharmacobio-Dyn. 4(9):724-734.
73. Toole BP 2004. Hyaluronan: From extracellular glue to pericellular cue. Nat Rev Cancer. 4(7):528-539.
74. Toole BP 2002. Hyaluronan promotes the malignant phenotype. Glycobiology. 12(3):37R-42R.
75. Vincent T, Jourdan M, Sy M-S, Klein B, Mechti N. 2001. Hyaluronic acid induces survival and proliferation of human myeloma cells through an interleukin-6-mediated pathway involving the phosphorylation of retinoblastoma protein. J Biol Chem. 276(18):14728-14736.
76. West DC, Hampson IN, Arnold F, Kumar S. 1985. Angiogenesis induced by degradation products of hyaluronic acid. Science. 228(4705):1324-1326.
77. Yoshihara S, Kon A, Kudo D, Nakazawa H, Kakizaki I, Sasaki M, Endo M, Takagaki K. 2005. A hyaluronan synthase suppressor, 4-methylumbelliferone, inhibits liver metastasis of melanoma cells. FEBS Lett. 579(12):2722-2726.
78. Zhu AX, Duda DG, Sahani DV, Jain RK. 2011. HCC and angiogenesis: Possible targets and future directions. Nat Rev Clin Oncol. 8(5):292-301.