Sulfatase 1 and sulfatase 2 in hepatocellular carcinoma: Associated signaling pathways, tumor phenotypes, and survival

Genes Chromosomes and Cancer

Volumn 50, Issue 2, 2011, Pages 122-135

  Yang, Ju Dong ^a   Sun, Zhifu ^a   Hu, Chunling ^a   Lai, Jinping ^a   Dove, Rebecca ^a   Nakamura, Ikuo ^a   Lee, Ju Seog ^b   Thorgeirsson, Snorri S ^c   Kang, Koo Jeong ^d   Chu, In Sun ^e   Roberts, Lewis R ^a  

^a MAYO CLINIC CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d Keimyung University School of Medicine   (South Korea)

^e Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; MESSENGER RNA; SULFATASE; SULFATASE 1; SULFATASE 2; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VIMENTIN; WNT PROTEIN;

ADULT; ARTICLE; BLOOD CLOTTING; CELL ADHESION; COMPUTER PROGRAM; CONTROLLED STUDY; CYTOSKELETON; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; LIVER CELL CARCINOMA; LIVER DEVELOPMENT; MAJOR CLINICAL STUDY; MALE; PHENOTYPE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN MICROARRAY; SIGNAL TRANSDUCTION; SURVIVAL;

CARCINOMA, HEPATOCELLULAR; DATABASES, GENETIC; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC ASSOCIATION STUDIES; HUMANS; LIVER NEOPLASMS; MALE; MICROARRAY ANALYSIS; PHENOTYPE; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SULFOTRANSFERASES; SURVIVAL ANALYSIS;

EID: 78649991362     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.20838     Document Type: Article

References (50)

1. Ai X, Do AT, Lozynska O, Kusche-Gullberg M, Lindahl U, Emerson CP, Jr. 2003. QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J Cell Biol 162: 341-351.
2. Battaglia S, Benzoubir N, Nobilet S, Charneau P, Samuel D, Zignego AL, Atfi A, Brechot C, Bourgeade MF. 2009. Liver cancer-derived hepatitis C virus core proteins shift TGF-beta responses from tumor suppression to epithelial-mesenchymal transition. PLoS One 4: e4355.
3. Benetti A, Berenzi A, Gambarotti M, Garrafa E, Gelati M, Dessy E, Portolani N, Piardi T, Giulini SM, Caruso A, Invernici G, Parati E, Nicosia R, Alessandri G. 2008. Transforming growth factor-beta1 and CD105 promote the migration of hepatocellular carcinoma-derived endothelium. Cancer Res 68: 8626-8634.
4. Briggs MW, Li Z, Sacks DB. 2002. IQGAP1-mediated stimulation of transcriptional co-activation by beta-catenin is modulated by calmodulin. J Biol Chem 277: 7453-7465.
5. Chau BN, Diaz RL, Saunders MA, Cheng C, Chang AN, Warrener P, Bradshaw J, Linsley PS, Cleary MA. 2009. Identification of SULF2 as a novel transcriptional target of p53 by use of integrated genomic analyses. Cancer Res 69: 1368-1374.
6. Coulouarn C, Factor VM, Thorgeirsson SS. 2008. Transforming growth factor-beta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer. Hepatology 47: 2059-2067.
7. Dai Y, Yang Y, MacLeod V, Yue X, Rapraeger AC, Shriver Z, Venkataraman G, Sasisekharan R, Sanderson RD. 2005. HSulf-1 and HSulf-2 are potent inhibitors of myeloma tumor growth in vivo. J Biol Chem 280: 40066-40073.
8. Danesin C, Agius E, Escalas N, Ai X, Emerson C, Cochard P, Soula C. 2006. Ventral neural progenitors switch toward an oligodendroglial fate in response to increased Sonic hedgehog (Shh) activity: Involvement of Sulfatase 1 in modulating Shh signaling in the ventral spinal cord. J Neurosci 26: 5037-5048.
9. Dhoot GK, Gustafsson MK, Ai X, Sun W, Standiford DM, Emerson CP, Jr. 2001. Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293: 1663-1666.
10. Dredge K, Hammond E, Davis K, Li CP, Liu L, Johnstone K, Handley P, Wimmer N, Gonda TJ, Gautam A, Ferro V, Bytheway I. 2010. The PG500 series: Novel heparan sulfate mimetics as potent angiogenesis and heparanase inhibitors for cancer therapy. Invest New Drugs 28: 276-283.
11. Fujita K, Takechi E, Sakamoto N, Sumiyoshi N, Izumi S, Miyamoto T, Matsuura S, Tsurugaya T, Akasaka K, Yamamoto T. 2010. HpSulf, a heparan sulfate 6-O-endosulfatase, is involved in the regulation of VEGF signaling during sea urchin development. Mech Dev 127: 235-245.
12. Ho YD, Joyal JL, Li Z, Sacks DB. 1999. IQGAP1 integrates Ca2+/calmodulin and Cdc42 signaling. J Biol Chem 274: 464-470.
13. Hong L, Sun H, Lv X, Yang D, Zhang J, Shi Y. 2010. Expression of periostin in the serum of NSCLC and its function on proliferation and migration of human lung adenocarcinoma cell line (A549) in vitro. Mol Biol Rep 37: 2285-2293.
14. Hoshida Y, Nijman SM, Kobayashi M, Chan JA, Brunet JP, Chiang DY, Villanueva A, Newell P, Ikeda K, Hashimoto M, et al. 2009. Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma. Cancer Res 69: 7385-7392.
15. Hossain MM, Hosono-Fukao T, Tang R, Sugaya N, van Kuppevelt TH, Jenniskens GJ, Kimata K, Rosen SD, Uchimura K. 2010. Direct detection of HSulf-1 and HSulf-2 activities on extracellular heparan sulfate and their inhibition by PI-88. Glycobiology 20: 175-186.
16. Hu L, Lau SH, Tzang CH, Wen JM, Wang W, Xie D, Huang M, Wang Y, Wu MC, Huang JF, Zeng WF, Sham JS, Yang M, Guan XY. 2004. Association of Vimentin overexpression and hepatocellular carcinoma metastasis. Oncogene 23: 298-302.
17. Iizuka N, Tamesa T, Sakamoto K, Miyamoto T, Hamamoto Y, Oka M. 2006. Different molecular pathways determining extrahepatic and intrahepatic recurrences of hepatocellular carcinoma. Oncol Rep 16: 1137-1142.
18. Kalus I, Salmen B, Viebahn C, von Figura K, Schmitz D, D'Hooge R, Dierks T. 2009. Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity. J Cell Mol Med 13: 4505-4521.
19. Kuroda S, Fukata M, Nakagawa M, Fujii K, Nakamura T, Ookubo T, Izawa I, Nagase T, Nomura N, Tani H, Shoji I, Matsuura Y, Yonehara S, Kaibuchi K. 1998. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin- mediated cell-cell adhesion. Science 281: 832-835.
20. Lai J, Chien J, Staub J, Avula R, Greene EL, Matthews TA, Smith DI, Kaufmann SH, Roberts LR, Shridhar V. 2003. Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer. J Biol Chem 278: 23107-23117.
21. Lai JP, Chien J, Strome SE, Staub J, Montoya DP, Greene EL, Smith DI, Roberts LR, Shridhar V. 2004a. HSulf-1 modulates HGF-mediated tumor cell invasion and signaling in head and neck squamous carcinoma. Oncogene 23: 1439-1447.
22. Lai JP, Chien JR, Moser DR, Staub JK, Aderca I, Montoya DP, Matthews TA, Nagorney DM, Cunningham JM, Smith DI, Greene EL, Shridhar V, Roberts LR. 2004b. hSulf1 Sulfatase promotes apoptosis of hepatocellular cancer cells by decreasing heparin-binding growth factor signaling. Gastroenterology 126: 231-248.
23. Lai JP, Yu C, Moser CD, Aderca I, Han T, Garvey TD, Murphy LM, Garrity-Park MM, Shridhar V, Adjei AA, Roberts LR. 2006. SULF1 inhibits tumor growth and potentiates the effects of histone deacetylase inhibitors in hepatocellular carcinoma. Gastroenterology 130: 2130-2144.
24. Lai JP, Sandhu DS, Yu C, Han T, Moser CD, Jackson KK, Guerrero RB, Aderca I, Isomoto H, Garrity-Park MM, Zou H, Shire AM, Nagorney DM, Sanderson SO, Adjei AA, Lee JS, Thorgeirsson SS, Roberts LR. 2008. Sulfatase 2 up-regulates glypican 3, promotes fibroblast growth factor signaling, and decreases survival in hepatocellular carcinoma. Hepatology 47: 1211-1222.
25. Lai JP, Oseini AM, Moser CD, Yu C, Elsawa SF, Hu C, Nakamura I, Han T, Aderca I, Isomoto H, Garrity-Park MM, Shire AM, Li J, Sanderson SO, Adjei AA, Fernandez-Zapico ME, Roberts LR. 2010. The oncogenic effect of sulfatase 2 in human hepatocellular carcinoma is mediated in part by glypican 3-dependent Wnt activation. Hepatology 52: 1680-1689.
26. Lamanna WC, Baldwin RJ, Padva M, Kalus I, Ten Dam G, van Kuppevelt TH, Gallagher JT, von Figura K, Dierks T, Merry CL. 2006. Heparan sulfate 6-O-endosulfatases: Discrete in vivo activities and functional co-operativity. Biochem J 400: 63-73.
27. Lazarevich NL, Cheremnova OA, Varga EV, Ovchinnikov DA, Kudrjavtseva EI, Morozova OV, Fleishman DI, Engelhardt NV, Duncan SA. 2004. Progression of HCC in mice is associated with a downregulation in the expression of hepatocyte nuclear factors. Hepatology 39: 1038-1047.
28. Lee JS, Heo J, Libbrecht L, Chu IS, Kaposi-Novak P, Calvisi DF, Mikaelyan A, Roberts LR, Demetris AJ, Sun Z, Nevens F, Roskams T, Thorgeirsson SS. 2006. A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 12: 410-416.
29. Lemjabbar-Alaoui H, van Zante A, Singer MS, Xue Q, Wang YQ, Tsay D, He B, Jablons DM, Rosen SD. 2010. Sulf-2, a heparan sulfate endosulfatase, promotes human lung carcinogenesis. Oncogene 29: 635-646.
30. Li J, Kleeff J, Abiatari I, Kayed H, Giese NA, Felix K, Giese T, Buchler MW, Friess H. 2005. Enhanced levels of Hsulf-1 interfere with heparin-binding growth factor signaling in pancreatic cancer. Mol Cancer 4: 14.
31. Lum DH, Tan J, Rosen SD, Werb Z. 2007. Gene trap disruption of the mouse heparan sulfate 6-O-endosulfatase gene, Sulf2. Mol Cell Biol 27: 678-688.
32. Mataraza JM, Briggs MW, Li Z, Entwistle A, Ridley AJ, Sacks DB. 2003. IQGAP1 promotes cell motility and invasion. J Biol Chem 278: 41237-41245.
33. Mishra L, Banker T, Murray J, Byers S, Thenappan A, He AR, Shetty K, Johnson L, Reddy EP. 2009. Liver stem cells and hepatocellular carcinoma. Hepatology 49: 318-329.
34. Morimoto-Tomita M, Uchimura K, Bistrup A, Lum DH, Egeblad M, Boudreau N, Werb Z, Rosen SD. 2005. Sulf-2, a proangiogenic heparan sulfate endosulfatase, is upregulated in breast cancer. Neoplasia 7: 1001-1010.
35. Murata M, Matsuzaki K, Yoshida K, Sekimoto G, Tahashi Y, Mori S, Uemura Y, Sakaida N, Fujisawa J, Seki T, Kobayashi K, Yokote K, Koike K, Okazaki K. 2009. Hepatitis B virus X protein shifts human hepatic transforming growth factor (TGF)-beta signaling from tumor suppression to oncogenesis in early chronic hepatitis B. Hepatology 49: 1203-1217.
36. Narita K, Staub J, Chien J, Meyer K, Bauer M, Friedl A, Ramakrishnan S, Shridhar V. 2006. HSulf-1 inhibits angiogenesis and tumorigenesis in vivo. Cancer Res 66: 6025-6032.
37. Narita K, Chien J, Mullany SA, Staub J, Qian X, Lingle WL, Shridhar V. 2007. Loss of HSulf-1 expression enhances autocrine signaling mediated by amphiregulin in breast cancer. J Biol Chem 282: 14413-14420.
38. Nawroth R, van Zante A, Cervantes S, McManus M, Hebrok M, Rosen SD. 2007. Extracellular sulfatases, elements of the Wnt signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells. PLoS One 2: e392.
39. Ren JG, Li Z, Sacks DB. 2008. IQGAP1 integrates Ca2+/calmodulin and B-Raf signaling. J Biol Chem 283: 22972-22982.
40. Roy M, Li Z, Sacks DB. 2004. IQGAP1 binds ERK2 and modulates its activity. J Biol Chem 279: 17329-17337.
41. Roy M, Li Z, Sacks DB. 2005. IQGAP1 is a scaffold for mitogen-activated protein kinase signaling. Mol Cell Biol 25: 7940-7952.
42. Ruan K, Bao S, Ouyang G. 2009. The multifaceted role of periostin in tumorigenesis. Cell Mol Life Sci 66: 2219-2230.
43. Schmidt VA, Chiariello CS, Capilla E, Miller F, Bahou WF. 2008. Development of hepatocellular carcinoma in Iqgap2-deficient mice is IQGAP1 dependent. Mol Cell Biol 28: 1489-1502.
44. Uchimura K, Morimoto-Tomita M, Bistrup A, Li J, Lyon M, Gallagher J, Werb Z, Rosen SD. 2006. HSulf-2, an extracellular endoglucosamine-6-sulfatase, selectively mobilizes heparin-bound growth factors and chemokines: Effects on VEGF, FGF-1, and SDF-1. BMC Biochem 7: 2.
45. Viviano BL, Paine-Saunders S, Gasiunas N, Gallagher J, Saunders S. 2004. Domain-specific modification of heparan sulfate by Qsulf1 modulates the binding of the bone morphogenetic protein antagonist Noggin. J Biol Chem 279: 5604-5611.
46. Wang Y, Wang A, Wang F, Wang M, Zhu M, Ma Y, Wu R. 2008. IQGAP1 activates Tcf signal independent of Rac1 and Cdc42 in injury and repair of bronchial epithelial cells. Exp Mol Pathol 85: 122-128.
47. Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY, Jia H, Ye Q, Qin LX, Wauthier E, Reid LM, Minato H, Honda M, Kaneko S, Tang ZY, Wang XW. 2009. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 136: 1012-1024.
48. Yin C, Lin Y, Zhang X, Chen YX, Zeng X, Yue HY, Hou JL, Deng X, Zhang JP, Han ZG, Xie WF. 2008. Differentiation therapy of hepatocellular carcinoma in mice with recombinant adenovirus carrying hepatocyte nuclear factor-4alpha gene. Hepatology 48: 1528-1539.
49. Yue X, Li X, Nguyen HT, Chin DR, Sullivan DE, Lasky JA. 2008. Transforming growth factor-beta1 induces heparan sulfate 6-O-endosulfatase 1 expression in vitro and in vivo. J Biol Chem 283: 20397-20407.
50. Zhou J, Liang S, Fang L, Chen L, Tang M, Xu Y, Fu A, Yang J, Wei Y. 2009. Quantitative proteomic analysis of HepG2 Cells treated with quercetin suggests IQGAP1 involved in quercetin-induced regulation of cell proliferation and migration. Omics 13: 93-103.