Heparan sulphate synthetic and editing enzymes in ovarian cancer - PubMed (original) (raw)
Comparative Study
. 2007 May 21;96(10):1544-8.
doi: 10.1038/sj.bjc.6603747. Epub 2007 Apr 17.
Affiliations
- PMID: 17437011
- PMCID: PMC2359940
- DOI: 10.1038/sj.bjc.6603747
Comparative Study
Heparan sulphate synthetic and editing enzymes in ovarian cancer
A C Backen et al. Br J Cancer. 2007.
Abstract
Several angiogenic growth factors including fibroblast growth factors 1 and 2 (FGF1 and FGF2) depend on heparan sulphate (HS) for biological activity. We previously showed that all cellular elements in ovarian tumour tissue synthesised HS but biologically active HS (i.e. HS capable of binding FGF2 and its receptor) was confined to ovarian tumour endothelium. In this study, we have sought to explain this observation. Heparan sulphate sulphotransferases 1 and 2 (HS6ST1 and HS6ST2) attach sulphate groups to C-6 of glucosamine residues in HS that are critical for FGF2 activation. These enzymes were strongly expressed by tumour cells, but only HS6ST1 was found in endothelial cells. Immunostaining with the 3G10 antibody of tissue sections pretreated with heparinases indicated that HS proteoglycans were produced by tumour and endothelial cells. These results indicated that, in contrast to the endothelium, HS produced by tumour cells may be modified by cell-surface heparanase (HPA1) or endosulphatase (SULF). Protein and RNA analysis revealed that HPA1 was strongly expressed by ovarian tumour cells in eight of ten specimens examined. HSULF-1, which removes specific 6-O-sulphate groups from HS, was abundant in tumour cells but weakly expressed in the endothelium. If this enzyme was responsible for the lack of biologically active HS on the tumour cell surface, we would expect exogenous FGF2 binding to be preserved; we showed previously that this was indeed the case although FGF2 binding was reduced compared to the endothelium and stroma. Thus, the combined effects of heparanase and HSULF could account for the lack of biologically active HS in tumour cells rather than deficiencies in the biosynthetic enzymes.
Figures
Figure 1
(A) HS6ST1 ISH shows RNA to be present in ovary tumour and endothelial cells, but absent in stroma and normal ovary (inset). (B) HS6ST2 ISH shows RNA to be present in ovary tumour cells, but absent in endothelial cells, stroma and normal ovary (inset). (C) 10E4, an anti-HS monoclonal antibody was used to demonstrate that intact HS chains were only present on endothelial cells in ovarian tumours. (D) 3G10 antibody was used to detect the HS stubs that remain after heparinase digestion. A negative control shows 3G10 staining to be negative without prior heparinase digestion (inset). (E) Heparanase ISH shows RNA to be present in ovary tumour cells, but absent in endothelial cells and stroma. (F) Heparanase IHC shows protein to be present in ovary tumour cells, but absent in endothelial cells and stroma. (G) Heparanase IHC on normal human ovary shows protein to be present at a low level in most cells. (H) HSULF-1 ISH shows RNA to be present in ovary tumour cells, but absent in endothelial cells, stroma and normal ovary (inset). Each scale bar represents 400 _μ_m.
Similar articles
- Endothelial heparan sulfate 6-O-sulfation levels regulate angiogenic responses of endothelial cells to fibroblast growth factor 2 and vascular endothelial growth factor.
Ferreras C, Rushton G, Cole CL, Babur M, Telfer BA, van Kuppevelt TH, Gardiner JM, Williams KJ, Jayson GC, Avizienyte E. Ferreras C, et al. J Biol Chem. 2012 Oct 19;287(43):36132-46. doi: 10.1074/jbc.M112.384875. Epub 2012 Aug 27. J Biol Chem. 2012. PMID: 22927437 Free PMC article. - Ovarian cancer cell heparan sulfate 6-O-sulfotransferases regulate an angiogenic program induced by heparin-binding epidermal growth factor (EGF)-like growth factor/EGF receptor signaling.
Cole CL, Rushton G, Jayson GC, Avizienyte E. Cole CL, et al. J Biol Chem. 2014 Apr 11;289(15):10488-10501. doi: 10.1074/jbc.M113.534263. Epub 2014 Feb 22. J Biol Chem. 2014. PMID: 24563483 Free PMC article. - Heparan Sulfate Biosynthetic System Is Inhibited in Human Glioma Due to EXT1/2 and HS6ST1/2 Down-Regulation.
Ushakov VS, Tsidulko AY, de La Bourdonnaye G, Kazanskaya GM, Volkov AM, Kiselev RS, Kobozev VV, Kostromskaya DV, Gaytan AS, Krivoshapkin AL, Aidagulova SV, Grigorieva EV. Ushakov VS, et al. Int J Mol Sci. 2017 Nov 1;18(11):2301. doi: 10.3390/ijms18112301. Int J Mol Sci. 2017. PMID: 29104277 Free PMC article. - Heparin-derived heparan sulfate mimics to modulate heparan sulfate-protein interaction in inflammation and cancer.
Casu B, Naggi A, Torri G. Casu B, et al. Matrix Biol. 2010 Jul;29(6):442-52. doi: 10.1016/j.matbio.2010.04.003. Epub 2010 Apr 21. Matrix Biol. 2010. PMID: 20416374 Free PMC article. Review. - Glucosaminyl N-deacetylase/N-sulphotransferases in heparan sulphate biosynthesis and biology.
Kjellén L. Kjellén L. Biochem Soc Trans. 2003 Apr;31(2):340-2. doi: 10.1042/bst0310340. Biochem Soc Trans. 2003. PMID: 12653633 Review.
Cited by
- Germline Sequencing Identifies Rare Variants in Finnish Subjects with Familial Germ Cell Tumors.
Crowgey EL, Soini T, Shah N, Pauniaho SL, Lahdenne P, Wilson DB, Heikinheimo M, Druley TE. Crowgey EL, et al. Appl Clin Genet. 2020 Jun 30;13:127-137. doi: 10.2147/TACG.S245093. eCollection 2020. Appl Clin Genet. 2020. PMID: 32636668 Free PMC article. - Selectins: An Important Family of Glycan-Binding Cell Adhesion Molecules in Ovarian Cancer.
Hassan AA, Artemenko M, Tang MKS, Wong AST. Hassan AA, et al. Cancers (Basel). 2020 Aug 10;12(8):2238. doi: 10.3390/cancers12082238. Cancers (Basel). 2020. PMID: 32785160 Free PMC article. Review. - Chemical Tumor Biology of Heparan Sulfate Proteoglycans.
Raman K, Kuberan B. Raman K, et al. Curr Chem Biol. 2010 Jan 1;4(1):20-31. doi: 10.2174/187231310790226206. Curr Chem Biol. 2010. PMID: 20596243 Free PMC article. - Silencing of S100A4, a metastasis-associated protein, in endothelial cells inhibits tumor angiogenesis and growth.
Ochiya T, Takenaga K, Endo H. Ochiya T, et al. Angiogenesis. 2014 Jan;17(1):17-26. doi: 10.1007/s10456-013-9372-7. Epub 2013 Aug 9. Angiogenesis. 2014. PMID: 23929008 Free PMC article.
References
- Ai X, Do AT, Kusche-Gullberg M, Lindahl U, Lu K, Emerson Jr CP (2006) Substrate specificity and domain functions of extracellular heparan sulfate 6-O-endosulfatases, QSulf1 and QSulf2. J Biol Chem 281(8): 4969–4976, doi:10.1074/jbc.M511902200 - PubMed
- Chang Z, Meyer K, Rapraeger AC, Friedl A. (2000) Differential ability of heparan sulfate proteoglycans to assemble the fibroblast growth factor receptor complex in situ. FASEB J 14(1): 137–144 - PubMed
- Davies EJ, Blackhall FH, Shanks JH, David G, McGown AT, Swindell R, Slade RJ, Martin-Hirsch P, Gallagher JT, Jayson GC (2004) Distribution and clinical significance of HS proteoglycans in ovarian cancer. Clin Cancer Res 10(15): 5178–5186 - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical