Specific genes involved in synthesis and editing of heparan sulfate proteoglycans show altered expression patterns in breast cancer

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Fernández Vega, Iván ^a   García, Olivia ^b   Crespo, Ainara ^c   Castañón, Sonia ^c   Menéndez, Primitiva ^a   Astudillo, Aurora ^a   Quirós, Luis M ^d  

^a HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

^b UNIVERSITY OF OVIEDO   (Spain)

^c NEIKER and a Vaccine producing Commercial Company CZVSL   (Spain)

^d DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

Author keywords

Breast cancer; Glycosaminoglycan; Heparan sulfate; Invasive ductal carcinoma; Proteoglycan

Indexed keywords

3 O SULFOTRANSFERASE; CHONDROITIN SULFATE; GLYPICAN 3; HEPARANASE; HEPARANASE 2; MESSENGER RNA; PERLECAN; PROTEIN NDST4; PROTEOHEPARAN SULFATE; SULFATASE; SULFOTRANSFERASE; SYNDECAN 1; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BREAST CARCINOMA; BREAST METASTASIS; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; PROTEIN EXPRESSION; PROTEIN PROCESSING; SULFATION;

BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CHONDROITIN SULFATES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCURONIDASE; GLYPICANS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; POLYMERASE CHAIN REACTION; RNA, MESSENGER; SULFOTRANSFERASES; SYNDECAN-1; TUMOR MARKERS, BIOLOGICAL;

EID: 84872274487     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-24     Document Type: Article

References (43)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin D. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010, 127:2893-2917. 10.1002/ijc.25516, 21351269.
2. Weaver VM, Gilbert P. Watch thy neighbor: cancer is a communal affair. J Cell Sci 2004, 117:1287-1290. 10.1242/jcs.01137, 15020668.
3. Löfgren L, Sahlin L, Jiang S, Von Schoultz B, Fernstad R, Skoog L, Von Schoultz E. Expression of syndecan-1 in paired samples of normal and malignant breast tissue from postmenopausal women. Anticancer Res 2007, 27:3045-3050.
4. Esko JD, Lindahl U. Molecular diversity of heparan sulphate. J Clin Invest 2001, 108:169-173. 203033, 11457867.
5. Whitelock JM, Iozzo RV. Heparan sulfate: a complex polymer charged with biological activity. Chem Rev 2005, 105:2745-2764. 10.1021/cr010213m, 16011323.
6. Park PW, Reizes O, Bernfields M. Cell surface heparan sulfate proteoglycans: selective regulators of ligand-receptor encounters. J Biol Chem 2000, 275:29923-29926.
7. Sanderson RD. Heparan sulfate proteoglycans in invasion and metastasis. Semin Cell Dev Biol 2001, 12:89-98. 10.1006/scdb.2000.0241, 11292374.
8. Iozzo RV, San Antonio J. Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J Clin Invest 2001, 108:349-355. 209371, 11489925.
9. Matsuda K, Maruyama H, Guo F, Kleeff J, Itakura J, Matsumoto Y, Lander AD, Korc M. Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells. Cancer Res 2001, 61:5562-5569.
10. Morimoto-Tomita M, Uchimura K, Bistrup A, Lum DH, Egeblad M, Boudreau N, Werb Z, Rosen SD. Sulf-2, a proangiogenic heparan sulfate endosulfatase, is upregulated in breast cancer. Neoplasia 2005, 7:1001-1010. 10.1593/neo.05496, 1502017, 16331886.
11. Narita K, Chien J, Mullany SA, Staub J, Qian X, Lingle WL, Shridhar V. Loss of HSulf-1 expression enhances autocrine signaling mediated by amphiregulin in breast cancer. J Biol Chem 2007, 282:14413-14420. 10.1074/jbc.M611395200, 17363371.
12. Miyamoto K, Asada K, Fukutomi T, Okochi E, Yagi Y, Hasegawa T, Asahara T, Sugimura T, Ushijima T. Methylation-associated silencing of heparan sulfate D-glucosaminyl 3-O-sulfotransferase-2 (3-OST-2) in human breast, colon, lung and pancreatic cancers. Oncogene 2003, 22:274-280. 10.1038/sj.onc.1206146, 12527896.
13. Raman K, Kuberan B. Chemical tumor biology of heparan sulfate proteoglycans. Curr Chem Biol 2010, 4:20-31. 2892923, 20596243.
14. Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H. Quantitative real-time RT-PCR data analysis: current concepts and the novel " gene expression's CT difference" formula. J Mol Med 2006, 84:901-910. 10.1007/s00109-006-0097-6, 16972087.
15. Iozzo RV. Heparan sulfate proteoglycans: intrincate molecules with intriguing functions. J Clin Invest 2001, 108:165-167. 203034, 11457866.
16. Lindahl U, Kusche-Gullberg M, Kjellén L. Regulated diversity of heparan sulphate. J Biol Chem 1998, 273:24979-24982. 10.1074/jbc.273.39.24979, 9737951.
17. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J 2006, 20:9-22. 10.1096/fj.05-4682rev, 16394262.
18. Nairn AV, Kinoshita-Toyoda A, Toyoda H, Xie J, Harris K, Dalton S, Kulik M, Pierce JM, Toida T, Moremen KW, Linhardt RJ. Glycomics of proteoglycan biosynthesis in murine embryonic stem cell differentiation. J Proteome Res 2007, 6:4374-4387. 10.1021/pr070446f, 17915907.
19. Dong J, Kukula AK, Toyoshima M, Nakajima M. Genomic structure and chromosome localization of the newly identified human heparanase gene. Gene 2000, 253:171-178. 10.1016/S0378-1119(00)00251-1, 10940554.
20. Arvatz G, Shafat I, Levy-Adam F, Ilan N, Vlodavsky I. The heparanase system and tumor metastasis: is heparanase the seed and soil?. Cancer Metast Rev 2011, 30:253-268.
21. Arvatz G, Barash U, Nativ O, Ilan N, Vlodavsky I. Post-transcriptional regulation of heparanase gene expression by a 3′AU-rich element. FASEB J 2010, 24:4969-4976. 10.1096/fj.10-156372, 3229425, 20798248.
22. Theocharis AD, Skandalis SS, Tzanakakis GN, Karamanos NK. Proteoglycans in health and disease: novel roles for proteoglycans in malignancy and their pharmacological targeting. FEBS J 2010, 277:3904-3923. 10.1111/j.1742-4658.2010.07800.x, 20840587.
23. Grobe K, Esko JD. Regulated translation of heparan sulfate N-acetylglucosamine N-deacetylase/N-sulfotransferase isozymes by structured 5′-untranslated regions and internal ribosome entry sites. J Biol Chem 2002, 277:30699-30706. 10.1074/jbc.M111904200, 12070138.
24. Yeaman C, Rapraeger AC. Post-transcriptional regulation of syndecan-1 expression by cAMP in peritoneal macrophages. J Cell Biol 1993, 122:941-950. 10.1083/jcb.122.4.941, 2119584, 8394371.
25. Lofgren L, Sahlin L, Jiang S, Von Schoultz B, Fernstad R, Skoog L, Von Schoultz E. Expression of syndecan-1 in paired samples of normal and malignant breast tissue from postmenopausal women. Anticancer Res 2007, 27:3045-3050.
26. Maeda T, Desouky J, Friedl A. Syndecan-1 expression by stromal fibroblasts promotes breast carcinoma growth in vivo and stimulates tumor angiogenesis. Oncogene 2006, 25:1408-1412. 10.1038/sj.onc.1209168, 16247452.
27. Yang N, Mosher R, Seo S, Beebe D, Friedl A. Syndecan-1 in breast cancer stroma fibroblasts regulates extracellular matrix fiber organization and carcinoma cell motility. Am J Pathol 2011, 178:325-335. 10.1016/j.ajpath.2010.11.039, 3069862, 21224069.
28. Baba F, Swartz K, van Buren R, Eickhoff J, Zhang Y, Wolberg W, Friedl A. Syndecan-1 and syndecan-4 are overexpressed in an estrogen receptor-negative, highly proliferative breast carcinoma subtype. Breast Cancer Res Tr 2006, 98:91-98.
29. Xiang YY, Ladeda V, Filmus J. Glypican-3 expression is silenced in human breast cancer. Oncogene 2001, 20:7408-7412. 10.1038/sj.onc.1204925, 11704870.
30. Iozzo RV, Zoeller JJ, Nyström A. Basement membrane proteoglycans: modulators Par Excellence of cancer growth and angiogenesis. Mol Cells 2009, 27:503-513. 10.1007/s10059-009-0069-0, 19466598.
31. Xinnong J, Couchman J. Perlecan and tumor angiogenesis. J Histochem Cytochem 2003, 51:1393-1410. 10.1177/002215540305101101, 14566013.
32. Takeuchi J, Sobue M, Sato E, Shamoto M, Miura K. Variation in glycosaminoglycan components of breast tumors. Cancer Res 1976, 36:2133-2139.
33. Grobe K, Ledin J, Ringvall M, Holmborn K, Forsberg E, Esko JD, Kjellén L. Heparan sulfate and development: differential roles of the N-acetylglucosamine N-deacetylase/N-sulfotransferase isozymes. Biochim Biophys Acta 2002, 1573:209-215. 10.1016/S0304-4165(02)00386-0, 12417402.
34. Aikawa J, Grobe K, Tsujimoto M, Esk JD. Multiple isozymes of heparan sulfate/heparin GlcNAc N-deacetylase/GlcN N-sulfotransferase. Structure and activity of the fourth member, NDST4. J Biol Chem 2001, 276:5876-5882. 10.1074/jbc.M009606200, 11087757.
35. Smeds E, Habuchi H, Do AT, Hjertson E, Grundberg H, Kimata K, Lindahl U, Kusche-Gullberg M. Substrate specificities of mouse heparan sulphate glucosaminyl 6-O-sulphotransferases. Biochem J 2003, 372:371-380. 10.1042/BJ20021666, 1223407, 12611590.
36. Bui C, Ouzzine M, Talhaoui I, Sharp S, Prydz K, Coughtrie MW, Fournel-Gigleux S. Epigenetics:methylation-associated repression of heparan sulfate 3-O-sulfotransferase gene expression contributes to the invasive phenotype of H-EMC-SS chondrosarcoma cells. FASEB J 2010, 24:436-450. 10.1096/fj.09-136291, 19812376.
37. Mochizuki H, Yoshida K, Shibata Y, Kimata K. Tetrasulfated disaccharide unit in heparan sulfate: enzymatic formation and tissue distribution. J Biol Chem 2008, 283:31237-31245. 10.1074/jbc.M801586200, 2662186, 18757372.
38. Lamanna WC, Kalus I, Padva M, Baldwin RJ, Merry CL, Dierks T. The heparanomed. The enigma of encoding and decoding heparan sulfate sulfation. J Biotechnol 2007, 129:290-307. 10.1016/j.jbiotec.2007.01.022, 17337080.
39. Troup S, Njue C, Kliewer EV, Parisien M, Roskelley C, Chakravarti S, Roughley PJ, Murphy LC, Watson PH. Reduced expression of the small leucine-rich proteoglycans, lumican, and decorin is associated with poor outcome in node-negative invasive breast cancer. Clin Cancer Res 2003, 9:207-214.
40. Cooney CA, Jousheghany F, Yao-Borengasser A, Phanavanh B, Gomes T, Kieber-Emmons AM, Siegel ER, Suva LJ, Ferrone S, Kieber-Emmons T, Monzavi-Karbassi B. Chondroitin sulfates play a major role in breast cancer metastasis: a role for CSPG4 and CHST11 gene expression in forming surface P-selectin ligands in aggressive breast cancer cells. Breast Cancer Res 2011, 13:R58. 10.1186/bcr2895, 3218947, 21658254.
41. Mikami T, Mizumoto S, Kago N, Kitagawa H, Sugahara K. Specificities of three distinct human chondroitin/dermatan N-acetylgalactosamine 4-O-sulfotransferases demonstrated using partially desulfated dermatan sulfate as an acceptor: implication of differential roles in dermatan sulfate biosynthesis. J Biol Chem 2003, 278:36115-36127. 10.1074/jbc.M306044200, 12847091.
42. Ilan N, Elkin M, Vlodavsky I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int J Biochem Cell Biol 2006, 38:2018-2039. 10.1016/j.biocel.2006.06.004, 16901744.
43. Levy-Adam F, Feld S, Cohen-Kaplan V, Shteingauz A, Gross M, Arvatz G, Naroditsky I, Ilan N, Doweck I, Vlodavsky I. Heparanase 2 interacts with heparan sulfate with high affinity and inhibits heparanase activity. J Biol Chem 2010, 285:28010-28019. 10.1074/jbc.M110.116384, 2934666, 20576607.