Hsulf-1 gene exhibits anticancer efficacy through negatively regulating VEGFR-2 signaling in human cancers

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Ji, Weidan ^a,b   Yang, Jiahe ^a   Wang, Duanming ^c   Cao, Lu ^a   Tan, Weifeng ^a   Qian, Haihua ^a   Sun, Bin ^a   Qian, Qijun ^a   Yin, Zhengfeng ^a   Wu, Mengchao ^a   Su, Changqing ^a,b  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^c SHIHEZI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; SHORT HAIRPIN RNA; SULFATASE; SULFATASE 1; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; SULF1 PROTEIN, HUMAN; SULFOTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD VESSEL PARAMETERS; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION; GENE FUNCTION; HSULF1 GENE; HUMAN; HUMAN CELL; INHIBITION KINETICS; LIVER CELL CARCINOMA; MICROVASCULAR DENSITY; MOUSE; NONHUMAN; NUDE MOUSE; OVARY CANCER; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; ADENOVIRUS; ANIMAL; BAGG ALBINO MOUSE; CELL SURVIVAL; DRUG SCREENING; ENZYME ACTIVATION; ENZYMOLOGY; GENE THERAPY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; NEOPLASM; PATHOLOGY; PHOSPHORYLATION; TREATMENT OUTCOME; TUMOR CELL LINE;

ADENOVIRIDAE; MUS MUSCULUS;

ADENOVIRIDAE; ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DOWN-REGULATION; ENZYME ACTIVATION; GENE THERAPY; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASMS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SULFOTRANSFERASES; TREATMENT OUTCOME; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 80051540053     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023274     Document Type: Article

References (35)

1. Liu D, Shriver Z, Qi Y, Venkataraman G, Sasisekharan R, (2002) Dynamic regulation of tumor growth and metastasis by heparan sulfate glycosaminoglycans. Semin Thromb Hemost 28: 67-78.
2. Sasisekharan R, Shriver Z, Venkataraman G, Narayanasami U, (2002) Roles of heparan-sulphate glycosaminoglycans in cancer. Nat Rev Cancer 2: 521-528.
3. Lemjabbar-Alaoui H, van Zante A, Singer MS, Xue Q, Wang YQ, et al. (2010) Sulf-2, a heparan sulfate endosulfatase, promotes human lung carcinogenesis. Oncogene 29: 635-646.
4. Lai JP, Sandhu DS, Shire AM, Roberts LR, (2008) The tumor suppressor function of human sulfatase 1 (SULF1) in carcinogenesis. J Gastrointest Cancer 39: 149-158.
5. Li J, Kleeff J, Abiatari I, Kayed H, Giese NA, et al. (2005) Enhanced levels of Hsulf-1 interfere with heparin-binding growth factor signaling in pancreatic cancer. Mol Cancer 4: 14.
6. Narita K, Staub J, Chien J, Meyer K, Bauer M, et al. (2006) HSulf-1 inhibits angiogenesis and tumorigenesis in vivo. Cancer Res 66: 6025-6032.
7. Narita K, Chien J, Mullany SA, Staub J, Qian X, et al. (2007) Loss of HSulf-1 expression enhances autocrine signaling mediated by amphiregulin in breast cancer. J Biol Chem 282: 14413-14420.
8. Chen Z, Fan JQ, Li J, Li QS, Yan Z, et al. (2009) Promoter hypermethylation correlates with the Hsulf-1 silencing in human breast and gastric cancer. Int J Cancer 124: 739-744.
9. Staub J, Chien J, Pan Y, Qian X, Narita K, et al. (2007) Epigenetic silencing of HSulf-1 in ovarian cancer: implications in chemoresistance. Oncogene 26: 4969-4978.
10. Liu P, Khurana A, Rattan R, He X, Kalloger S, et al. (2009) Regulation of HSulf-1 expression by variant hepatic nuclear factor 1 in ovarian cancer. Cancer Res 69: 4843-4850.
11. Lai J, Chien J, Staub J, Avula R, Greene EL, et al. (2003) Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer. J Biol Chem 278: 23107-23117.
12. Lai JP, Yu C, Moser CD, Aderca I, Han T, et al. (2006) SULF1 inhibits tumor growth and potentiates the effects of histone deacetylase inhibitors in hepatocellular carcinoma. Gastroenterology 130: 2130-2144.
13. Guo S, Colbert LS, Fuller M, Zhang Y, Gonzalez-Perez RR, (2010) Vascular endothelial growth factor receptor-2 in breast cancer. Biochim Biophys Acta 1806: 108-121.
14. Hossain MM, Hosono-Fukao T, Tang R, Sugaya N, van Kuppevelt TH, et al. (2010) Direct detection of HSulf-1 and HSulf-2 activities on extracellular heparan sulfate and their inhibition by PI-88. Glycobiology 20: 175-186.
15. Nawroth R, van Zante A, Cervantes S, McManus M, Hebrok M, et al. (2007) Extracellular sulfatases, elements of the Wnt signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells. PLoS One 2: e392.
16. Morimoto-Tomita M, Uchimura K, Werb Z, Hemmerich S, Rosen SD, (2002) Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J Biol Chem 277: 49175-49185.
17. Yue X, Li X, Nguyen HT, Chin DR, Sullivan DE, et al. (2008) Transforming growth factor-beta1 induces heparan sulfate 6-O-endosulfatase 1 expression in vitro and in vivo. J Biol Chem 283: 20397-20407.
18. Abiatari I, Kleeff J, Li J, Felix K, Büchler MW, et al. (2006) Hsulf-1 regulates growth and invasion of pancreatic cancer cells. J Clin Pathol 59: 1052-1058.
19. Rapraeger AC, Guimond S, Krufka A, Olwin BB, (1994) Regulation by heparan sulfate in fibroblast growth factor signaling. Methods Enzymol 245: 219-240.
20. Lai JP, Chien JR, Moser DR, Staub JK, Aderca I, et al. (2004) hSulf1 Sulfatase promotes apoptosis of hepatocellular cancer cells by decreasing heparin-binding growth factor signaling. Gastroenterology 126: 231-248.
21. Lai JP, Thompson JR, Sandhu DS, Roberts LR, (2008B) Heparin-degrading sulfatases in hepatocellular carcinoma: roles in pathogenesis and therapy targets. Future Oncol 4: 803-814.
22. Zhao TT, Trinh D, Addison CL, Dimitroulakos J, (2010) Lovastatin inhibits VEGFR and AKT activation: synergistic cytotoxicity in combination with VEGFR inhibitors. PLoS One 5: e12563.
23. Senger DR, Van de Water L, Brown LF, Nagy JA, Yeo KT, et al. (1993) Vascular permeability factor (VPF, VEGF) in tumor biology. Cancer Metastasis Rev 12: 303-324.
24. Byrne AM, Bouchier-Hayes DJ, Harmey JH, (2005) Angiogenic and cell survival functions of vascular endothelial growth factor (VEGF). J Cell Mol Med 9: 777-794.
25. Lichtenberger BM, Tan PK, Niederleithner H, Ferrara N, Petzelbauer P, et al. (2010) Autocrine VEGF signaling synergizes with EGFR in tumor cells to promote epithelial cancer development. Cell 140: 268-279.
26. Thakker GD, Hajjar DP, Muller WA, Rosengart TK, (1999) The role of phosphatidylinositol 3-kinase in vascular endothelial growth factor signaling. J Biol Chem 274: 10002-10007.
27. Berra E, Pagès G, Pouysségur J, (2000) MAP kinases and hypoxia in the control of VEGF expression. Cancer Metastasis Rev 19: 139-145.
28. Perego P, Cossa G, Zuco V, Zunino F, (2010) Modulation of cell sensitivity to antitumor agents by targeting survival pathways. Biochem Pharmacol 80: 1459-1465.
29. Weigand M, Hantel P, Kreienberg R, Waltenberger J, (2005) Autocrine vascular endothelial growth factor signalling in breast cancer. Evidence from cell lines and primary breast cancer cultures in vitro. Angiogenesis 8: 197-204.
30. Soker S, Goldstaub D, Svahn CM, Vlodavsky I, Levi BZ, et al. (1994) Variations in the size and sulfation of heparin modulate the effect of heparin on the binding of VEGF165 to its receptors. Biochem Biophys Res Commun 203: 1339-1347.
31. Sakurai Y, Ohgimoto K, Kataoka Y, Yoshida N, Shibuya M, (2005) Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in vasculogenesis in mice. Proc Natl Acad Sci USA 102: 1076-1081.
32. LaBarre DD, Lowy RJ, (2001) Improvements in methods for calculating virus titer estimates from TCID50 and plaque assays. J Virol Methods 96: 107-126.
33. Hu H, Li Z, Chen J, Wang D, Ma J, et al. (2011) P16 reactivation induces anoikis and exhibits antitumour potency by downregulating Akt/survivin9 signalling in hepatocellular carcinoma cells. Gut 60: 710-721.
34. Fang L, Pu YY, Hu XC, Sun LJ, Luo HM, et al. (2010) Antiangiogenesis gene armed tumor-targeting adenovirus yields multiple antitumor activities in human HCC xenografts in nude mice. Hepatol Res 40: 216-228.
35. Uzzan B, Nicolas P, Cucherat M, Perret GY, (2004) Microvessel density as a prognostic factor in women with breast cancer: a systematic review of the literature and meta-analysis. Cancer Res 64: 2941-2955.