Article Data

  • Views 515
  • Dowloads 129

Original Research

Open Access

Syndecan-1 serves as a marker for the progression of epithelial ovarian carcinoma

  • Q. Guo1
  • X. Yang2
  • Y. Ma1
  • L. Ma1,3,*,

1Department of Obstetrics and Gynecology, Shengjing Hospital of China Medical University, Shenyang, China

2Department of Pharmacy, The First Hospital of Guangzhou Medical College, Guangzhou, China

3Center for Reproductive Medicine, The Third Affiliated Hospital of Sun Yat-sen University, Guangzhou, China

DOI: 10.12892/ejgo2688.2015 Vol.36,Issue 5,October 2015 pp.506-513

Published: 10 October 2015

*Corresponding Author(s): L. Ma E-mail: malin8@mail.sysu.edu.cn

Abstract

Purpose: Syndecan-1 (SDC-1) promotes the proliferation of cancer cells and plays a role in angiogenesis by binding to a variety of extracellular effectors. The present study was designed to compare the expression of SDC-1 in the normal ovary and in ovarian tumors, to better understand its roles in the progression of epithelial ovarian carcinoma (EOC). Materials and Methods: The expression of SDC- 1, fibroblast growth factor 2 (FGF-2), and FGF receptor 1 (FGFR1) and their transcripts in 65 samples including the normal ovary, benign tumors, borderline ovarian tumors, and EOC was assessed using immunohistochemistry and the reverse transcription-polymerase chain reaction. The influence of FGF-2 on the expression of SDC-1 mRNA syndecan-1 in a human ovarian carcinoma cell line was determined using an FGF-2-neutralizing antibody. Results: SDC-1 was not detected in normal ovarian tissue but was present in the epithelial cells of benign or borderline tumors and in ovarian adenocarcinomas. The levels of expression were significantly different in ovarian tissues derived from benign or malignant cases. Coordinate stromal expression of SDC-1 and its mRNA was detected at the original site of the tumor, as well as in metastatic foci in the greater omentum of ovarian adenocarcinomas. FGF-2 reduced the level of expression of SDC-1 mRNA when added exogenously to SKOV3 cells. This effect was abolished in the presence of an FGF-2-neutralizing antibody. Conclusion: SDC-1 contributes to the role of FGF-2 in proliferation and angiogenesis but may also play a role in the invasive properties of EOC. To the present authors’ knowledge, this study is the first to report the presence of distinct patterns of expression of SDC-1 in local and metastatic foci in the greater omentum in patients with EOC. These data reinforce the role of the tumor stroma in the invasive properties of ovarian adenocarcinoma and suggest that stromal changes in the expression of SDC-1 may originate from the stroma and contribute to the pathogenesis and metastatic potential of EOC.

Keywords

Syndecan-1; FGF-2; FGFR1; Ovarian carcinoma.

Cite and Share

Q. Guo,X. Yang,Y. Ma,L. Ma. Syndecan-1 serves as a marker for the progression of epithelial ovarian carcinoma. European Journal of Gynaecological Oncology. 2015. 36(5);506-513.

References

[1] Blackhall F.H., Merry C.L., Davies E.J., Jayson G.C.: “Heparan sul-fate proteoglycans and cancer”. Br. J. Cancer, 2001, 85, 1094.

[2] Sanderson R.D.: “Heparan sulfate proteoglycans in invasion and metastasis”. Semin. Cell. Dev. Biol., 2001, 12, 89.

[3] Gonzalez A.D., Kaya M., Shi W., Song H., Testa J.R., Penn L.Z., Fil-mus J.: “OCI-5/GPC3, a glypican encoded by a gene that is mutated in the Simpson-Golabi-Behmel overgrowth syndrome, induces apop-tosis in a cell line-specific manner”. J. Cell. Biol., 1998, 141, 1407.

[4] Filmus J.: “Glypicans in growth control and cancer”. Glycobiology, 2001, 11, 19R.

[5] Lin H., Huber R., Schlessinger D., Morin P.J.: “Frequent silencing of the GPC3 gene in ovarian cancer cell lines”. Cancer Res., 1999, 59, 807.

[6] Midorikawa Y., Ishikawa S., Iwanari H., Imamura T., Sakamoto H., Miyazono K., et al.: “Glypican-3, overexpressed in hepatocellular carcinoma, modulates FGF2 and BMP-7 signalling”. Int. J. Cancer, 2003, 103, 455.

[7] Powell C.A., Xu G., Filmus J., Busch S., Brody J.S., Rothman P.B.: “Oligonucleotide microarray analysis of lung adenocarcinoma in smokers and nonsmokers identifies GPC3 as a potential lung tumor suppressor”. Chest, 2002, 12, 6S.

[8] Xiang Y.Y., Ladeda V., Filmus J.: “Glypican-3 expression is silenced in human breast cancer”. Oncogene, 2001, 20, 7408.

[9] Kokenyesi R.: “Ovarian carcinoma cells synthesize both chondroitin sulfate and heparan sulfate cell surface proteoglycans that mediate cell adhesion to interstitial matrix”. J. Cell. Biochem., 2001, 83, 259.

[10] International Collaborative Ovarian Neoplasm Group: “Paclitaxel plus carboplatin versus standard chemotherapy with either single-agent carboplatin or cyclophosphamide, doxorubicin, and cisplatin in women with ovarian cancer, the ICON3 randomised trial”. Lancet, 2002, 360, 505.

[11] Kato M., Wang H., Kainulainen V., Fitzgerald M.L., Ledbetter S., Ornitz D.M., Bernfield M.: “Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activa-tor of FGF-2”. Nat. Med., 1998, 4, 691.

[12] Fitzgerald M.L., Wang Z., Park P.W., Murphy G., Bernfield M.: “Shedding of syndecan-1 and -4 ectodomains is regulated by multi-ple signaling pathways and mediated by a TIMP-3-sensitive metal-loproteinase”. J. Cell. Biol., 2000, 148, 811.

[13] Presta M., Leali D., Stabile H., Ronca R., Camozzi M., Coco L., et al.: “Heparin derivatives as angiogenesis inhibitors”. Curr. Pharm. Des., 2003, 9, 553.

[14] Davies E.J., Blackhall F.H., Shanks J.H., David G., McGown A.T., Swindell R., et al.: “Distribution and clinical significance of heparan sulfate proteoglycans in ovarian cancer”. Clin. Cancer Res., 2004, 10, 5178.

[15] Ridley R.C., Xiao H.Q., Hata H., Woodliff J., Epstein J., Sanderson R. D.: “Expression of syndecan regulates human myeloma plasma cell adhesion to type I collagen”. Blood, 1993, 81, 767.

[16] Wijdenes J., Vooijs W.C., Clément C., Post J., Morard F., Vita N.,et al.: “A plasmocyte selective monoclonal antibody (B-B4) recognizes syndecan-1”. Br. J. Haematol., 1996, 94, 318.

[17] Perrimon N., Bernfield M.: “Specificities of heparan sulphate pro-teoglycans in developmental processes”. Nature, 2000, 404, 725.

[18] Rapraeger A.C.: “Molecular interactions of syndecans during devel-opment”. Semin. Cell. Dev. Biol., 2001, 12, 107.

[19] Carey D.J.: “Syndecans: multifunctional cell-surface co-receptors”. Biochem. J., 1997, 327,1.

[20] Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M.: “Functions of cell surface heparan sulfate proteoglycans”. Ann. Rev. Biochem., 1999, 68, 729.

[21] Liebersbach B.F., Sanderson R.D.: “Expression of syndecan-1 inhibits cell invasion into type I collagen”. J. Biol. Chem., 1994, 269, 20013.

[22] Ohashi M., Kusumi T., Sato F.: “Expression of syndecan-1 and E-cadherin is inversely correlated with poor patient’s prognosis and re-current status of extrahepatic bile duct carcinoma”. Biomed. Res., 2009, 30, 79.

[23] Kato M., Saunders S., Nguyen H., Bernfield M.: “Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells”. Mol. Biol. Cell., 1995, 6, 559.

[24] Barbareschi M., Maisonneuve P., Aldovini D., Cangi M.G., Peccia-rini L., Angelo Mauri F., et al.: “High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis”. Cancer 2003, 98, 474.

[25] Davies E.J., Blackhall F.H., Shanks J.H., David G., McGown A.T., Swindell R., et al.: “Distribution and clinical significance of heparan sulfate proteoglycans in ovarian cancer”. Clin. Cancer Res., 2004, 10, 5178.

[26] Conejo J.R., Kleeff J., Koliopanos A., Matsuda K., Zhu Z.W., Goecke H., et al.: “Syndecan-1 expression is up-regulated in pan-creatic but not in other gastrointestinal cancers”. Int. J. Cancer, 2000, 88, 12.

[27] Watanabe A., Mabuchi T., Satoh E., Furuya K., Zhang L., Maeda S., Naganuma H.: “Expression of syndecans, a heparan sulfate proteo-glycan in malignant gliomas: participation of nuclear factor-kappaB in upregulation of syndecan-1 expression”. J. Neurooncol., 2006, 77, 25.

[28] Conejo J.R., Kleeff J., Koliopanos A., Matsuda K., Zhu Z.W., Goecke H., et al.: “Syndecan-1 expression is up-regulated in pan-creatic but not in other gastrointestinal cancers”. Int. J. Cancer, 2000, 88, 12.

[29] Chen D., Adenekan B., Chen L.: “Syndecan-1 expression in locally invasive and metastatic prostate cancer”. Urology, 2004, 63, 402.

[30] Anttonen A., Heikkila P., Kajanti M., Jalkanen M., Joensuu H.: “High syndecan-1 expression is associated with favourable outcome in squamous cell lung carcinoma treated with radical surgery”. Lung Cancer, 2001, 32, 297.

[31] Numa F., Hirabayashi K., Kawasaki K., Sakaguchi Y., Sugino N., Suehiro Y., et al.: “Syndecan-1 expression in cancer of the uterine cervix: association with lymph node metastasis”. Int. J. Oncol., 2002, 20, 39.

[32] Rintala M., Inki P., Klemi P., Jalkanen M., Grénman S.: “Association of syndecan-1 with tumor grade and histology in primary invasive cervical carcinoma”. Gynecol. Oncol., 1999, 75, 372.

[33] Inki P., Stenback F., Grenman S., Jalkanen M.: “Immunohistochem-ical localization of syndecan-1 in normal and pathological human uterine cervix”. J. Pathol., 1994, 172, 349.

[34] Leppä S., Vleminckx K., Van Roy F.: “Syndecan-1 expression in mammary epithelial tumor cells is E-cadherin-independent”. J. Cell Sci., 1996, 109, 1393.

[35] Mennerich D., Vogel A., Klaman I., Dahl E., Lichtner R.B., Rosen-thal A., et al.: “Shift of syndecan-1 expression from epithelial to stro-mal cells during progression of solid tumours”. Eur. J. Cancer, 2004, 40, 1373.

[36] Chen L., Sanderson R.D.: “Heparanase regulates levels of syndecan-1 in the nucleus”. PLoS One, 2009, 4, e4947.

[37] Nikolova V., Koo C.Y., Ibrahim S.A., Wang Z., Spillmann D., Dreier R., et al.: “Differential roles for membrane-bound and soluble syndecan-1 (CD138) in breast cancer progression”. Carcinogenesis, 2009, 30, 397.

[38] Krypta R.: “Cell junctions, cell adhesion, and the extracellular ma-trix”. In: Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Wal-ter P., (eds). Molecular Biology of the Cell, 4th ed. New York: Garland Publishing, 2002, 1131.

[39] Hughes S.E.: “Differential expression of the fibroblast growth fac-tor receptor (FGFR) multigene family in normal human adult tis-sues”. J. Histochem. Cytochem., 1997, 45, 1005.

[40] Guddo F., Fontanini G., Reina C., Vignola A.M., Angeletti A., Bon-signore G.: “The expression of basic fibroblast growth factor (bFGF) in tumor associated stromal cells and vessels is inversely correlated with non small cell lung cancer progression”. Hum. Pathol., 1999, 30, 788.

[41] Iida S., Katoh O., Tokunaga A., Terada M.: “Expression of fibroblast growth factor gene family and its receptor gene family in the human upper gastrointestinal tract”. Biochem. Biophys. Res. Commun., 1996, 199, 1113.

[42] Fujimoto J., Ichigo S., Hori M., Hirose R., Sakaguchi H., Tamaya T.: “Expression of basic fibroblast growth factor and its mRNA in ad-vanced uterine cervical cancers”. Cancer Lett., 1997, 111, 21.

[43] Fujimoto J., Hori M., Ichigo S., Tamaya T.: “Expressions of the fi-broblast growth factor family (FGF-1, -2 and -4) mRNA in en-dometrial cancers”. Tumour Biol., 1996, 17, 226.

[44] Fujimoto J., Ichigo S., Hori M., Hirose R., Sakaguchi H., Tamaya T.: “Expression of basic fibroblast growth factor and its mRNA in ad-vanced ovarian cancers”. Eur. J. Gynaecol. Oncol., 1997, 18, 349.

[45] Couchman J.R.: “Syndecans: proteoglycan regulators of cell surface microdomains?” Nat. Rev. Mol. Cell. Biol., 2003, 4, 926.

[46] Kumar-Singh S., Jacobs W., Dhaene K., Weyn B., Bogers J., Weyler J., Van Marck E.: “Syndecan-1 expression in malignant mesothe-lioma: correlation with cell differentiation, WT1 expression, and clinical outcome”. J. Pathol., 1998, 186, 300.

[47] Maeda T., Desouky J., Friedl A.: “Syndecan-1 expression by stro-mal fibroblasts promotes breast carcinoma growth in vivo and stim-ulates tumor angiogenesis”. Oncogene, 2006, 25, 1408.

[48] Joensuu H., Anttonen A., Eriksson M., Mäkitaro R., Alfthan H., Kin-nula V., Leppä S.: “Soluble syndecan-1 and serum basic fibroblast growth factor are new prognostic factors in lung cancer”. Cancer Res., 2002, 62, 5210.

[49] Mahtouk K., Hose D., Raynaud P., Hundemer M., Jourdan M., Jour-dan E., et al.: “Heparanase influences expression and shedding of syndecan-1, and its expression by the bone marrow environment is a bad prognostic factor in multiple myeloma”. Blood, 2007, 109, 4914.

[50] Blackhall F.H., Merry C.L., Davies E.J., Jayson G.C.: “Heparan sul-fate proteoglycans and cancer”. Br. J. Cancer, 2001, 85, 1094.

[51] Stanley M.J., Stanley M.W., Sanderson R.D., Zera R.: “Syndecan-1 expression is induced in the stroma of infiltrating breast carci-noma”. Am. J. Clin. Pathol., 1999, 112, 377.

Abstracted / indexed in

Science Citation Index Expanded (SciSearch) Created as SCI in 1964, Science Citation Index Expanded now indexes over 9,500 of the world’s most impactful journals across 178 scientific disciplines. More than 53 million records and 1.18 billion cited references date back from 1900 to present.

Biological Abstracts Easily discover critical journal coverage of the life sciences with Biological Abstracts, produced by the Web of Science Group, with topics ranging from botany to microbiology to pharmacology. Including BIOSIS indexing and MeSH terms, specialized indexing in Biological Abstracts helps you to discover more accurate, context-sensitive results.

Google Scholar Google Scholar is a freely accessible web search engine that indexes the full text or metadata of scholarly literature across an array of publishing formats and disciplines.

JournalSeek Genamics JournalSeek is the largest completely categorized database of freely available journal information available on the internet. The database presently contains 39226 titles. Journal information includes the description (aims and scope), journal abbreviation, journal homepage link, subject category and ISSN.

Current Contents - Clinical Medicine Current Contents - Clinical Medicine provides easy access to complete tables of contents, abstracts, bibliographic information and all other significant items in recently published issues from over 1,000 leading journals in clinical medicine.

BIOSIS Previews BIOSIS Previews is an English-language, bibliographic database service, with abstracts and citation indexing. It is part of Clarivate Analytics Web of Science suite. BIOSIS Previews indexes data from 1926 to the present.

Journal Citation Reports/Science Edition Journal Citation Reports/Science Edition aims to evaluate a journal’s value from multiple perspectives including the journal impact factor, descriptive data about a journal’s open access content as well as contributing authors, and provide readers a transparent and publisher-neutral data & statistics information about the journal.

Submission Turnaround Time

Conferences

Top