The tumor suppressor function of human sulfatase 1 (SULF1) in carcinogenesis

Journal of Gastrointestinal Cancer

Volumn 39, Issue 1-4, 2008, Pages 149-158

  Lai, Jin Ping ^a   Sandhu, Dalbir S ^a   Shire, Abdirashid M ^a   Roberts, Lewis R ^a  

^a MAYO CLINIC   (United States)

Author keywords

Methylation; SULF1; Sulfatase; Tumor suppressor

Indexed keywords

APICIDIN; CISPLATIN; DOXORUBICIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; HISTONE DEACETYLASE INHIBITOR; HUMAN SULFATASE 1; PLATELET DERIVED GROWTH FACTOR; PROTEIN TYROSINE KINASE; PROTEOHEPARAN SULFATE; SCATTER FACTOR; STAUROSPORINE; SULFATASE; UNCLASSIFIED DRUG; VASCULOTROPIN; FIBROBLAST GROWTH FACTOR RECEPTOR; HISTONE DEACETYLASE; SULF1 PROTEIN, HUMAN; SULFOTRANSFERASE; TUMOR SUPPRESSOR PROTEIN; VASCULOTROPIN A;

ANGIOGENESIS; APOPTOSIS; BREAST CANCER; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; DNA METHYLATION; HUMAN; KNOCKOUT MOUSE; LIVER CELL CARCINOMA; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SULF1 GENE; SULFATION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; DRUG ANTAGONISM; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

APOPTOSIS; DNA METHYLATION; FIBROBLAST GROWTH FACTOR 2; HEPARAN SULFATE PROTEOGLYCANS; HEPATOCYTE GROWTH FACTOR; HISTONE DEACETYLASES; HUMANS; MAP KINASE SIGNALING SYSTEM; NEOPLASMS; RECEPTORS, FIBROBLAST GROWTH FACTOR; SULFOTRANSFERASES; TUMOR SUPPRESSOR PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 69849092570     PISSN: 19416628     EISSN: 19416636     Source Type: Journal    
DOI: 10.1007/s12029-009-9058-y     Document Type: Review

References (34)

1. G Diez-Roux A Ballabio 2005 Sulfatases and human disease Annu Rev Genomics Hum Genet 6 355 379 10.1146/annurev.genom.6.080604.162334 16124866 10.1146/annurev.genom.6.080604.162334 1:CAS:528:DC%2BD2MXhtFWisrvI (Pubitemid 41397088)
2. V Shridhar A Sen J Chien J Staub R Avula S Kovats, et al. 2002 Identification of underexpressed genes in early- and late-stage primary ovarian tumors by suppression subtraction hybridization Cancer Res 62 1 262 270 11782386 1:CAS:528:DC%2BD38XntV2gsg%3D%3D
3. X Ai AT Do M Kusche-Gullberg U Lindahl K Lu CP Emerson Jr 2006 Substrate specificity and domain functions of extracellular heparan sulfate 6-O-endosulfatases, QSulf1 and QSulf2 J Biol Chem 281 8 4969 4976 10.1074/jbc.M511902200 16377625 10.1074/jbc.M511902200 1:CAS:528: DC%2BD28Xhs1eksbk%3D (Pubitemid 43847759)
4. GK Dhoot MK Gustafsson X Ai W Sun DM Standiford CP Emerson Jr 2001 Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase Science 293 5535 1663 1666 10.1126/science.293.5535.1663 11533491 10.1126/science.293.5535.1663 1:CAS:528:DC%2BD3MXms1Chsbg%3D (Pubitemid 32807846)
5. J Lai J Chien J Staub R Avula EL Greene TA Matthews, et al. 2003 Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer J Biol Chem 278 25 23107 23117 10.1074/jbc.M302203200 12686563 10.1074/jbc.M302203200 1:CAS:528:DC%2BD3sXksF2hsrY%3D (Pubitemid 36830377)
6. JP Lai JR Chien DR Moser JK Staub I Aderca DP Montoya, et al. 2004 hSulf1 sulfatase promotes apoptosis of hepatocellular cancer cells by decreasing heparin-binding growth factor signaling Gastroenterology 126 1 231 248 10.1053/j.gastro.2003.09.043 14699503 10.1053/j.gastro.2003.09.043 1:CAS:528:DC%2BD2cXhtFGntbg%3D (Pubitemid 38040739)
7. K Forsten-Williams CL Chu M Fannon JA Buczek-Thomas MA Nugent 2008 Control of growth factor networks by heparan sulfate proteoglycans Ann Biomed Eng 36 12 2134 2148 10.1007/s10439-008-9575-z 18839312 10.1007/s10439-008-9575-z
8. R Kikuno T Nagase K Ishikawa M Hirosawa N Miyajima A Tanaka, et al. 1999 Prediction of the coding sequences of unidentified human genes. XIV. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro DNA Res 6 3 197 205 10.1093/dnares/6.3.197 10470851 10.1093/dnares/6.3.197 1:CAS:528:DyaK1MXkslKmtbc%3D (Pubitemid 129705079)
9. M Morimoto-Tomita K Uchimura Z Werb S Hemmerich SD Rosen 2002 Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans J Biol Chem 277 51 49175 49185 10.1074/jbc.M205131200 12368295 10.1074/jbc.M205131200 1:CAS:528:DC%2BD38XpsFalur4%3D (Pubitemid 36014346)
10. T Ohto H Uchida H Yamazaki K Keino-Masu A Matsui M Masu 2002 Identification of a novel nonlysosomal sulphatase expressed in the floor plate, choroid plexus and cartilage Genes Cells 7 2 173 185 10.1046/j.1356-9597.2001. 00502.x 11895481 10.1046/j.1356-9597.2001.00502.x 1:CAS:528:DC%2BD38XisVKnsLw%3D (Pubitemid 34213362)
11. J Staub J Chien Y Pan X Qian K Narita G Aletti, et al. 2007 Epigenetic silencing of HSulf-1 in ovarian cancer: implications in chemoresistance Oncogene 26 34 4969 4978 10.1038/sj.onc.1210300 17310998 10.1038/sj.onc.1210300 1:CAS:528:DC%2BD2sXotFygs7s%3D (Pubitemid 47172647)
12. JP Lai J Chien SE Strome J Staub DP Montoya EL Greene, et al. 2004 HSulf-1 modulates HGF-mediated tumor cell invasion and signaling in head and neck squamous carcinoma Oncogene 23 7 1439 1447 10.1038/sj.onc.1207258 14973553 10.1038/sj.onc.1207258 1:CAS:528:DC%2BD2cXhtlKhurw%3D (Pubitemid 38406839)
13. K Narita J Chien SA Mullany J Staub X Qian WL Lingle, et al. 2007 Loss of HSulf-1 expression enhances autocrine signaling mediated by amphiregulin in breast cancer J Biol Chem 282 19 14413 14420 10.1074/jbc.M611395200 17363371 10.1074/jbc.M611395200 1:CAS:528:DC%2BD2sXkvVynsbk%3D (Pubitemid 47100479)
14. J Li J Kleeff I Abiatari H Kayed NA Giese K Felix, et al. 2005 Enhanced levels of Hsulf-1 interfere with heparin-binding growth factor signaling in pancreatic cancer Mol Cancer 4 1 14 10.1186/1476-4598-4-14 15817123 10.1186/1476-4598-4-14 (Pubitemid 41460844)
15. R Nawroth A van Zante S Cervantes M McManus M Hebrok SD Rosen 2007 Extracellular sulfatases, elements of the Wnt signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells PLoS ONE 2 4 e392 10.1371/journal.pone.0000392 17460759 10.1371/journal.pone.0000392
16. HD Soule TM Maloney SR Wolman WD Peterson Jr R Brenz CM McGrath, et al. 1990 Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10 Cancer Res 50 18 6075 6086 1975513 1:CAS:528:DyaK3MXktFSq
17. SH Cross JA Charlton X Nan AP Bird 1994 Purification of CpG islands using a methylated DNA binding column Nat Genet 6 3 236 244 10.1038/ng0394-236 8012384 10.1038/ng0394-236 1:CAS:528:DyaK2cXktVajt7Y%3D (Pubitemid 24188619)
18. Z Chen JQ Fan J Li QS Li Z Yan XK Jia, et al. 2009 Promoter hypermethylation correlates with the Hsulf-1 silencing in human breast and gastric cancer Int J Cancer 124 3 739 744 10.1002/ijc.23960 19006069 10.1002/ijc.23960 1:CAS:528:DC%2BD1MXmt1Glug%3D%3D
19. X Ai AT Do O Lozynska M Kusche-Gullberg U Lindahl CP Emerson Jr 2003 QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling J Cell Biol 162 2 341 351 10.1083/jcb.200212083 12860968 10.1083/jcb.200212083 1:CAS:528: DC%2BD3sXlvVCgu7o%3D (Pubitemid 36928846)
20. L Lundin H Larsson J Kreuger S Kanda U Lindahl M Salmivirta, et al. 2000 Selectively desulfated heparin inhibits fibroblast growth factor-induced mitogenicity and angiogenesis J Biol Chem 275 32 24653 24660 10.1074/jbc.M908930199 10816596 10.1074/jbc.M908930199 1:CAS:528: DC%2BD3cXlsl2jsb8%3D (Pubitemid 30626565)
21. M Delehedde M Lyon JT Gallagher PS Rudland DG Fernig 2002 Fibroblast growth factor-2 binds to small heparin-derived oligosaccharides and stimulates a sustained phosphorylation of p42/44 mitogen-activated protein kinase and proliferation of rat mammary fibroblasts Biochem J 366 Pt 1 235 244 12000311 1:CAS:528:DC%2BD3sXptFOhtL4%3D
22. S Wang X Ai SD Freeman ME Pownall Q Lu DS Kessler, et al. 2004 QSulf1, a heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis Proc Natl Acad Sci USA 101 14 4833 4838 10.1073/pnas.0401028101 15051888 10.1073/pnas.0401028101 1:CAS:528: DC%2BD2cXjsFCjurc%3D (Pubitemid 38469163)
23. G Dong Z Chen ZY Li NT Yeh CC Bancroft C Van Waes 2001 Hepatocyte growth factor/scatter factor-induced activation of MEK and PI3K signal pathways contributes to expression of proangiogenic cytokines interleukin-8 and vascular endothelial growth factor in head and neck squamous cell carcinoma Cancer Res 61 15 5911 5918 11479233 1:CAS:528:DC%2BD3MXlvVCgu70%3D
24. G Dong TL Lee NT Yeh J Geoghegan C Van Waes Z Chen 2004 Metastatic squamous cell carcinoma cells that overexpress c-Met exhibit enhanced angiogenesis factor expression, scattering and metastasis in response to hepatocyte growth factor Oncogene 23 37 6199 6208 10.1038/sj.onc.1207851 15221009 10.1038/sj.onc.1207851 1:CAS:528:DC%2BD2cXmslCmtLw%3D (Pubitemid 39215290)
25. K Matsumoto K Matsumoto T Nakamura RH Kramer 1994 Hepatocyte growth factor/scatter factor induces tyrosine phosphorylation of focal adhesion kinase (p125FAK) and promotes migration and invasion by oral squamous cell carcinoma cells J Biol Chem 269 50 31807 31813 7527397 1:CAS:528:DyaK2cXmvFemtLk%3D
26. E Galeazzi M Olivero FC Gervasio A De Stefani G Valente PM Comoglio, et al. 1997 Detection of MET oncogene/hepatocyte growth factor receptor in lymph node metastases from head and neck squamous cell carcinomas Eur Arch Otorhinolaryngol 254 Suppl 1 S138 S143 10.1007/BF02439745 9065649 10.1007/BF02439745 (Pubitemid 27110381)
27. K Narita J Staub J Chien K Meyer M Bauer A Friedl, et al. 2006 HSulf-1 inhibits angiogenesis and tumorigenesis in vivo Cancer Res 66 12 6025 6032 10.1158/0008-5472.CAN-05-3582 16778174 10.1158/0008-5472.CAN-05-3582 1:CAS:528:DC%2BD28XlvVSlu7k%3D
28. JP Lai C Yu CD Moser I Aderca T Han TD Garvey, et al. 2006 SULF1 inhibits tumor growth and potentiates the effects of histone deacetylase inhibitors in hepatocellular carcinoma Gastroenterology 130 7 2130 2144 10.1053/j.gastro.2006. 02.056 16762634 10.1053/j.gastro.2006.02.056 1:CAS:528:DC%2BD28XntVWit7Y%3D (Pubitemid 43816959)
29. Lai J-P, Sandhu D, Moser C, Cazanave S, Oseini A, Shire A, Shridhar V, Sanderson S, Roberts L. Additive effect of apicidin and doxorubicin in sulfatase 1 (SULF1)-expressing hepatocellular carcinoma in vitro and in vivo. J Hepatol. 2009; in press.
30. I Abiatari J Kleeff J Li K Felix MW Buchler H Friess 2006 Hsulf-1 regulates growth and invasion of pancreatic cancer cells J Clin Pathol 59 10 1052 1058 10.1136/jcp.2005.031716 16603650 10.1136/jcp.2005.031716 1:CAS:528:DC%2BD28Xht1SgtrfN (Pubitemid 44570327)
31. Q Dai SB Qian HH Li H McDonough C Borchers D Huang, et al. 2005 Regulation of the cytoplasmic quality control protein degradation pathway by BAG2 J Biol Chem 280 46 38673 38681 10.1074/jbc.M507986200 16169850 10.1074/jbc.M507986200 1:CAS:528:DC%2BD2MXht1SktLjO (Pubitemid 43853770)
32. KV Butler AP Kozikowski 2008 Chemical origins of isoform selectivity in histone deacetylase inhibitors Curr Pharm Des 14 6 505 528 10.2174/ 138161208783885353 18336297 10.2174/138161208783885353 1:CAS:528: DC%2BD1cXksVGksbw%3D
33. WC Lamanna RJ Baldwin M Padva I Kalus G Ten Dam TH van Kuppevelt, et al. 2006 Heparan sulfate 6-O-endosulfatases: discrete in vivo activities and functional co-operativity Biochem J 400 1 63 73 10.1042/BJ20060848 16901266 10.1042/BJ20060848 1:CAS:528:DC%2BD28XhtFaksLnM (Pubitemid 44763820)
34. WC Lamanna MA Frese M Balleininger T Dierks 2008 Sulf loss influences N-, 2-O-, and 6-O-sulfation of multiple heparan sulfate proteoglycans and modulates fibroblast growth factor signaling J Biol Chem 283 41 27724 27735 10.1074/jbc.M802130200 18687675 10.1074/jbc.M802130200 1:CAS:528: DC%2BD1cXhtF2hsLbM