Up-regulated expression of sulfatases (SULF1 and SULF2) as prognostic and metastasis predictive markers in human gastric cancer

Journal of Pathology

Volumn 228, Issue 1, 2012, Pages 88-98

  Hur, Keun ^a,b   Han, Tae Su ^a   Jung, Eun Jung ^a   Yu, Jieun ^a   Lee, Hyuk Joon ^a   Kim, Woo Ho ^a   Goel, Ajay ^b   Yang, Han Kwang ^a  

^a Seoul National University College of Medicine   (South Korea)

^b BAYLOR RESEARCH INSTITUTE   (United States)

Author keywords

gastric cancer; hypomethylation; predictive marker; prognostic marker; SULF

Indexed keywords

SULF1 ENZYME; SULF2 ENZYME; SULFATASE; UNCLASSIFIED DRUG;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CANCER RECURRENCE; CONTROLLED STUDY; DISEASE MARKER; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; METHYLATION; MOUSE; NONHUMAN; OVERALL SURVIVAL; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH CANCER; TUMOR GROWTH; TUMOR XENOGRAFT; UPREGULATION;

ADENOCARCINOMA; AGED; ANIMALS; CELL LINE, TUMOR; CPG ISLANDS; DNA METHYLATION; FEMALE; GASTRIC MUCOSA; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPH NODES; LYMPHATIC METASTASIS; MALE; MICE; MICE, INBRED C57BL; MICE, NUDE; MIDDLE AGED; NEOPLASM STAGING; NEOPLASMS, EXPERIMENTAL; PROGNOSIS; STOMACH NEOPLASMS; SULFOTRANSFERASES; SURVIVAL RATE; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84864748547     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4055     Document Type: Article

References (30)

1. Parkin DM, Bray F, Ferlay J, et al., Global cancer statistics, 2002. CA Cancer J Clin 2005; 55: 74-108.
2. Yasui W, Oue N, Aung PP, et al., Molecular-pathological prognostic factors of gastric cancer: a review. Gastric Cancer 2005; 8: 86-94.
3. Bernfield M, Gotte M, Park PW, et al., Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 1999; 68: 729-777.
4. Dhoot GK, Gustafsson MK, Ai X, et al., Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 2001; 293: 1663-1666.
5. Morimoto-Tomita M, Uchimura K, Werb Z, et al., Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J Biol Chem 2002; 277: 49175-49185.
6. Lai J, Chien J, Staub J, et al., Loss of HSULF1 up-regulates heparin-binding growth factor signaling in cancer. J Biol Chem 2003; 278: 23107-23117.
7. Lai JP, Chien JR, Moser DR, et al., hSulf1 sulfatase promotes apoptosis of hepatocellular cancer cells by decreasing heparin-binding growth factor signaling. Gastroenterology 2004; 126: 231-248.
8. Li J, Kleeff J, Abiatari I, et al., Enhanced levels of HSULF1 interfere with heparin-binding growth factor signaling in pancreatic cancer. Mol Cancer 2005; 4: 14.
9. Ai X, Kitazawa T, Do AT, et al., SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation. Development 2007; 134: 3327-3338.
10. Viviano BL, Paine-Saunders S, Gasiunas N, et al., Domain-specific modification of heparan sulfate by Qsulf1 modulates the binding of the bone morphogenetic protein antagonist Noggin. J Biol Chem 2004; 279: 5604-5611.
11. Castro NP, Osorio CA, Torres C, et al., Evidence that molecular changes in cells occur before morphological alterations during the progression of breast ductal carcinoma. Breast Cancer Res 2008; 10: R87.
12. Grigoriadis A, Mackay A, Reis-Filho JS, et al., Establishment of the epithelial-specific transcriptome of normal and malignant human breast cells based on MPSS and array expression data. Breast Cancer Res 2006; 8: R56.
13. Lemjabbar-Alaoui H, van Zante A, Singer MS, et al., SULF2, a heparan sulfate endosulfatase, promotes human lung carcinogenesis. Oncogene 2010; 29: 635-646.
14. Kaiser S, Park YK, Franklin JL, et al., Transcriptional recapitulation and subversion of embryonic colon development by mouse colon tumor models and human colon cancer. Genome Biol 2007; 8: R131.
15. Kudo Y, Ogawa I, Kitajima S, et al., Periostin promotes invasion and anchorage-independent growth in the metastatic process of head and neck cancer. Cancer Res 2006; 66: 6928-6935.
16. Lai JP, Sandhu DS, Yu C, et al., Sulfatase 2 up-regulates glypican 3, promotes fibroblast growth factor signaling, and decreases survival in hepatocellular carcinoma. Hepatology 2008; 47: 1211-1222.
17. Jones PA, Baylin SB,. The epigenomics of cancer. Cell 2007; 128: 683-692.
18. Ushijima T, Sasako M,. Focus on gastric cancer. Cancer Cell 2004; 5: 121-125.
19. Hur K, Song SH, Lee HS, et al., Aberrant methylation of the specific CpG island portion regulates cyclooxygenase-2 gene expression in human gastric carcinomas. Biochem Biophys Res Commun 2003; 310: 844-851.
20. Chen Z, Fan JQ, Li J, et al., Promoter hypermethylation correlates with the HSULF1 silencing in human breast and gastric cancer. Int J Cancer 2009; 124: 739-744.
21. Junnila S, Kokkola A, Mizuguchi T, et al., Gene expression analysis identifies over-expression of CXCL1, SPARC, SPP1, and SULF1 in gastric cancer. Genes Chromosomes Cancer 2010; 49: 28-39.
22. Ai X, Do AT, Lozynska O, et al., QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J Cell Biol 2003; 162: 341-351.
23. Akiyama Y, Maesawa C, Ogasawara S, et al., Cell-type-specific repression of the maspin gene is disrupted frequently by demethylation at the promoter region in gastric intestinal metaplasia and cancer cells. Am J Pathol 2003; 163: 1911-1919.
24. Oshimo Y, Nakayama H, Ito R, et al., Promoter methylation of cyclin D2 gene in gastric carcinoma. Int J Oncol 2003; 23: 1663-1670.
25. Yanagawa N, Tamura G, Honda T, et al., Demethylation of the synuclein gamma gene CpG island in primary gastric cancers and gastric cancer cell lines. Clin Cancer Res 2004; 10: 2447-2451.
26. Sato N, Maehara N, Su GH, et al., Effects of 5-aza-2'-deoxycytidine on matrix metalloproteinase expression and pancreatic cancer cell invasiveness. J Natl Cancer Inst 2003; 95: 327-330.
27. Hossain MM, Hosono-Fukao T, Tang R, et al., Direct detection of HSULF1 and HSULF2 activities on extracellular heparan sulfate and their inhibition by PI-88. Glycobiology 2010; 20: 175-186.
28. Khachigian LM, Parish CR,. Phosphomannopentaose sulfate (PI-88): heparan sulfate mimetic with clinical potential in multiple vascular pathologies. Cardiovasc Drug Rev 2004; 22: 1-6.
29. Kudchadkar R, Gonzalez R, Lewis KD,. PI-88: a novel inhibitor of angiogenesis. Expert Opin Investig Drugs 2008; 17: 1769-1776.
30. Liu CJ, Lee PH, Lin DY, et al., Heparanase inhibitor PI-88 as adjuvant therapy for hepatocellular carcinoma after curative resection: a randomized phase II trial for safety and optimal dosage. J Hepatol 2009; 50: 958-968.