Antitumor effects of hyaluronic acid inhibitor 4-methylumbelliferone in an orthotopic hepatocellular carcinoma model in mice

Glycobiology

Volumn 22, Issue 3, 2012, Pages 400-410

  Piccioni, Flavia ^a,b   Malvicini, Mariana ^a,b   Garcia, Mariana G ^a,b   Rodriguez, Andrés ^a   Atorrasagasti, Catalina ^a,b   Kippes, Nestor ^a   Piedra Buena, Ignacio T ^a   Rizzo, Manglio M ^a   Bayo, Juan ^a,c   Aquino, Jorge ^a,b   Viola, Manuela ^d   Passi, Alberto ^d   Alaniz, Laura ^a,b   Mazzolini, Guillermo ^a,b  

^a UNIVERSIDAD AUSTRAL   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c ANPCyT   (Argentina)

^d UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

4 methylumbelliferone; liver cancer; liver fibrosis

Indexed keywords

HYMECROMONE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; FIBROGENESIS; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY INFILTRATE; LIVER CELL CARCINOMA; LIVER FIBROSIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STELLATE CELL; TUMOR GROWTH;

ANIMALS; ANTIGENS, CD44; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG SCREENING ASSAYS, ANTITUMOR; FIBROBLASTS; GLUCURONOSYLTRANSFERASE; HUMANS; HYALURONIC ACID; HYMECROMONE; LIVER; LIVER CIRRHOSIS, EXPERIMENTAL; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, INBRED C3H; NEOPLASM TRANSPLANTATION; THIOACETAMIDE; TUMOR BURDEN;

ANIMALIA; MUS;

EID: 84856244394     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwr158     Document Type: Article

References (42)

1. Alaniz L, Garcia MG, Gallo-Rodriguez C, Agusti R, Sterin-Speziale N, Hajos SE, Alvarez E. 2006. Hyaluronan oligosaccharides induce cell death through PI3-K/Akt pathway independently of NF-κB transcription factor. Glycobiology. 16:359-367.
2. Alaniz L, Garcia M, Rizzo M, Piccioni F, Mazzolini G. 2009. Altered hyaluronan biosynthesis and cancer progression: An immunological perspective. Mini Rev Med Chem. 9:1538-1546.
3. Bataller R, Brenner DA. 2005. Liver fibrosis. J Clin Invest. 115:209-218. (Pubitemid 40385459)
4. Beaussier M, Wendum D, Fouassier L, Rey C, Barbu V, Lasnier E, Lienhart A, Scoazec JY, Rosmorduc O, Housset C. 2005. Adaptative bile duct proliferative response in experimental bile duct ischemia. J Hepatol. 42:257-265. (Pubitemid 40143474)
5. Boregowda RK, Appaiah HN, Siddaiah M, Kumarswamy SB, Sunila S, Thimmaiah KN, Mortha K, Toole B, Banerjee S. 2006. Expression of hyaluronan in human tumor progression. J Carcinog. 5:2.
6. Cordo-Russo R, Garcia MG, Barrientos G, Orsal AS, Viola M, Moschansky P, Ringel F, Passi A, Alaniz L, Hajos S, et al. 2009. Murine abortion is associated with enhanced hyaluronan expression and abnormal localization at the fetomaternal interface. Placenta. 30:88-95.
7. Day AJ, Prestwich GD. 2002. Hyaluronan-binding proteins: Tying up the giant. J Biol Chem. 277:4585-4588. (Pubitemid 34968483)
8. De Smet K, Beken S, Vanhaecke T, Pauwels M, Vercruysse A, Rogiers V. 1998. Isolation of rat hepatocytes. Methods Mol Biol. 107:295-301.
9. El-Serag HB, Rudolph KL. 2007. Hepatocellular carcinoma: Epidemiology and molecular carcinogenesis. Gastroenterology. 132:2557-2576. (Pubitemid 46890874)
10. Engstrom-Laurent A, Loof L, Nyberg A, Schroder T. 1985. Increased serum levels of hyaluronate in liver disease. Hepatology. 5:638-642. (Pubitemid 15029737)
11. Fraser JR, Laurent TC, Laurent UB. 1997. Hyaluronan: Its nature, distribution, functions and turnover. J Intern Med. 242:27-33. (Pubitemid 27323862)
12. Fraser JR, Laurent TC, Pertoft H, Baxter E. 1981. Plasma clearance, tissue distribution and metabolism of hyaluronic acid injected intravenously in the rabbit. Biochem J. 200:415-424. (Pubitemid 12218264)
13. Frebourg T, Delpech B, Bercoff E, Senant J, Bertrand P, Deugnier Y, Bourreille J. 1986. Serum hyaluronate in liver diseases: Study by enzymoimmunological assay. Hepatology. 6:392-395. (Pubitemid 16086624)
14. Friedman SL. 2008. Mechanisms of hepatic fibrogenesis. Gastroenterology. 134:1655-1669. (Pubitemid 351615417)
15. George J, Tsutsumi M, Takase S. 2004. Expression of hyaluronic acid in N-nitrosodimethylamine induced hepatic fibrosis in rats. Int J Biochem Cell Biol. 36:307-319. (Pubitemid 37487765)
16. Guo N, Li X, Mann MM, Funderburgh ML, Du Y, Funderburgh JL. 2010. Hyaluronan synthesis mediates the fibrotic response of keratocytes to transforming growth factor beta. J Biol Chem. 285:32012-32019.
17. Jameson JM, Cauvi G, Sharp LL, Witherden DA, Havran WL. 2005. Gammadelta T cell-induced hyaluronan production by epithelial cells regulates inflammation. J Exp Med. 201:1269-1279. (Pubitemid 40629070)
18. Kakizaki I, Kojima K, Takagaki K, Endo M, Kannagi R, Ito M, Maruo Y, Sato H, Yasuda T, Mita S, et al. 2004. A novel mechanism for the inhibition of hyaluronan biosynthesis by 4-methylumbelliferone. J Biol Chem. 279:33281-33289. (Pubitemid 39062975)
19. Kornek M, Raskopf E, Tolba R, Becker U, Klöckner M, Sauerbruch T, Schmitz V. 2008. Accelerated orthotopic hepatocellular carcinomas growth is linked to increased expression of pro-angiogenic and prometastatic factors in murine liver fibrosis. Liver Int. 28:509-518. (Pubitemid 351411137)
20. 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. 315:1914-1923.
21. 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. 70:2613-2623.
22. McKee CM, Penno MB, Cowman M, Burdick MD, Strieter RM, Bao C, Noble PW. 1996. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J Clin Invest. 98:2403-2413. (Pubitemid 26394217)
23. Morohashi H, Kon A, Nakai M, Yamaguchi M, Kakizaki I, Yoshihara S, Sasaki M, Takagaki K. 2006. Study of hyaluronan synthase inhibitor, 4-methylumbelliferone derivatives on human pancreatic cancer cell (KP1-NL). Biochem Biophys Res Commun. 345:1454-1459. (Pubitemid 43817894)
24. Noble PW. 2002. Hyaluronan and its catabolic products in tissue injury and repair. Matrix Biol. 21:25-29. (Pubitemid 34100819)
25. Pons-Renedo F, Llovet JM. 2003. Hepatocellular carcinoma: A clinical update. MedGenMed. 5:11.
26. Rampone B, Schiavone B, Confuorto G. 2010. Current management of hepatocellular cancer. Curr Oncol Rep. 12:186-192.
27. Safadi R, Friedman SL. 2002. Hepatic fibrosis-role of hepatic stellate cell activation. MedGenMed. 4:27.
28. Salguero Palacios R, Roderfeld M, Hemmann S, Rath T, Atanasova S, Tschuschner A, Gressner OA, Weiskirchen R, Graf J, Roeb E. 2008. Activation of hepatic stellate cells is associated with cytokine expression in thioacetamide-induced hepatic fibrosis in mice. Lab Invest. 88: 1192-1203.
29. Stern R. 2005. Hyaluronan metabolism: A major paradox in cancer biology. Pathol Biol (Paris). 53:372-382. (Pubitemid 41112071)
30. Takeda S, Aburada M. 1981. The choleretic mechanism of coumarin compounds and phenolic compounds. J Pharmacobiodyn. 4:724-734. (Pubitemid 12234249)
31. Tammi MI, Day AJ, Turley EA. 2002. Hyaluronan and homeostasis: A balancing act. J Biol Chem. 277:4581-4584. (Pubitemid 34968482)
32. Toole BP. 2002. Hyaluronan promotes the malignant phenotype. Glycobiology. 12:37R-42R. (Pubitemid 34567859)
33. Toole BP. 2004. Hyaluronan: From extracellular glue to pericellular cue. Nat Rev Cancer. 4:528-539. (Pubitemid 38868622)
34. Turley EA, Noble PW, Bourguignon LY. 2002. Signaling properties of hyaluronan receptors. J Biol Chem. 277:4589-4592. (Pubitemid 34968484)
35. Twarock S, Freudenberger T, Poscher E, Dai G, Jannasch K, Dullin C, Alves F, Prenzel K, Knoefel WT, Stoecklein NH, et al. 2011. Inhibition of oesophageal squamous cell carcinoma progression by in vivo targeting of hyaluronan synthesis. Mol Cancer. 10:30.
36. Urakawa H, Nishida Y, Wasa J, Arai E, Zhuo L, Kimata K, Kozawa E, Futamura N, Ishiguro N. 2011. Inhibition of hyaluronan synthesis in breast cancer cells by 4-methylumbelliferone suppresses tumorigenicity in vitro and metastatic lesions of bone in vivo. Int J Cancer. doi: 10.1002/ijc.26014.
37. Urashima S, Tsutsumi M, Shimanaka K, Ueshima Y, Tsuchishima M, Itoh T, Kawahara H, Takase S. 1999. Histochemical study of hyaluronate in alcoholic liver disease. Alcohol Clin Exp Res. 23:56S-60S. (Pubitemid 29203200)
38. Vrochides D, Papanikolaou V, Pertoft H, Antoniades AA, Heldin P. 1996. Biosynthesis and degradation of hyaluronan by nonparenchymal liver cells during liver regeneration. Hepatology. 23:1650-1655. (Pubitemid 26181250)
39. Webber J, Jenkins RH, Meran S, Phillips A, Steadman R. 2009a. Modulation of TGFbeta1-dependent myofibroblast differentiation by hyaluronan. Am J Pathol. 175:148-160.
40. Webber J, Meran S, Steadman R, Phillips A. 2009b. Hyaluronan orchestrates transforming growth factor-β1-dependent maintenance of myofibroblast phenotype. J Biol Chem. 284:9083-9092.
41. West DC, Shaw DM, Lorenz P, Adzick NS, Longaker MT. 1997. Fibrotic healing of adult and late gestation fetal wounds correlates with increased hyaluronidase activity and removal of hyaluronan. Int J Biochem Cell Biol. 29:201-210. (Pubitemid 27096433)
42. 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: 2722-2726. (Pubitemid 40615683)