Tissue-specificity of proteoglycans expression in different cancers
https://doi.org/10.17650/2313-805X.2016.3.1.53-60
Abstract
Background. Proteoglycans (PGs) are complex glycosylated molecules playing an important role in cell-cell and cell-matrix interactions and signaling. Expression of PGs and their expression pattern change considerably during malignant transformation of mammalian cells and tissues.
Objective. The aim of our work was to investigate tissue-specificity of main PGs expression (glypican-1, perlecan, syndecan-1, aggrecan, versican, CSPG4/NG2, brevican, decorin, lumican) in normal cells (fibroblasts and normal epithelial prostate cells PNT2) and in different human cancer cell lines (prostate, breast, lung, brain, kidney). Expression patterns of main PGs were determined in these cells using reverse transcription polymerase chain reaction analysis and immunocytochemical staining.
Results. It was shown that fibroblasts actively expressed PGs, and PNT2 cells had lower (5–6-fold) expression levels of a limited set of PG. In different cancer cell lines, overall transcriptional activities of PGs varied up to 10-fold, although their expression patterns had tissue-specific properties (for example, expression of syndecan-1 is more specific for prostate cancer cells, while perlecan is typical for lung cancer cell lines).
Conclusions. Along with this, variability of the PG expression patterns in cell lines of the same tissue of origin was shown, suggesting a possible contribution of the variable PGs expression to intratumoural heterogeneity of cancer cells and their potential as perspective biomarker (s) for personalised cancer diagnostics.
About the Authors
A. V. Suhovskih
Institute of Molecular Biology and Biophysics;
Novosibirsk State University
Russian Federation
Russian Federation
2/12 Timakova St., Novosibirsk, 630117;
2 Pirogova St., Novosibirsk, 630090
E. V. Grigor’eva
Institute of Molecular Biology and Biophysics;
Novosibirsk State University
Russian Federation
Russian Federation
2/12 Timakova St., Novosibirsk, 630117;
2 Pirogova St., Novosibirsk, 630090
References
1. Sarrazin S., Lamanna W.C., Esko J.D. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol 2011;3(7):pii:a004952.
2. Theocharis A.D., Skandalis S.S., Tzanakakis G.N., Karamanos N.K. Proteoglycans in health and disease: novel roles for proteoglycans in malignancy and their pharmacological targeting. FEBS J 2010;277:3904–23.
3. Dietrich C.P., Nader H.B., Straus A.H. Structural differences of heparan sulfates according to the tissue and species of origin. Biochem Biophys Res Commun 1983;111(3):865–71.
4. Gharbaran R. Advances in the molecular functions of syndecan-1 (SDC1/CD138) in the pathogenesis of malignancies. Crit Rev Oncol Hematol 2015;94(1):1–17.
5. Liu W., Litwack E.D., Stanley M.J. et al. Heparan sulfate proteoglycans as adhesive and anti-invasive molecules. Syndecans and glypican have distinct functions. J Biol Chem 1998;273:22825–32.
6. Beauvais D.M., Burbach B.J., Rapraeger A.C. The syndecan-1 ectodomain regulates alphavbeta3 integrin activity in human mammary carcinoma cells. J Cell Biol 2004;167:171–81.
7. Shi X., Liang W., Yang W., et al. Decorin is responsible for progression of non-smallcell lung cancer by promoting cell proliferation and metastasis. Tumour Biol 2015;36(5):3345–54.
8. Iozzo R.V., Sanderson R.D. Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J Cell Mol Med 2011;15(5):1013–31.
9. Gotte M., Kersting C., Ruggiero M. et al. Predictive value of syndecan-1 expression for the response to neoadjuvant chemotherapy of primary breast cancer. Anticancer Res 2006;26:621–7.
10. Juuti A., Nordling S., Lundin J. et al. Syndecan-1 expression – a novel prognostic marker in pancreatic cancer. Oncology 2005;68(2–3):97–106.
11. Wiksten J.P., Lundin J., Nordling S. et al. Epithelial and stromal syndecan-1 expression as predictor of outcome in patients with gastric cancer. Int J Cancer 2001;95:1–6.
12. Hasengaowa, Kodama J., Kusumoto T. et al. Prognostic significance of syndecan-1 expression in human endometrial cancer. Ann Oncol 2005;16(7):1109–15.
13. Kusumoto T., Kodama J., Seki N. et al. Clinical significance of syndecan-1 and versican expression in human epithelial ovarian cancer. Oncol Rep 2010;23:917–25.
14. Ibrahim S.A., Hassan H., Vilardo L. et al. Syndecan-1 (CD138) modulates triple-negative breast cancer stem cell properties via regulation of LRP-6 and IL-6-mediated STAT3 signaling. PloS One 2013;8(12):e85737.
15. Kim S.Y., Choi E.J., Yun J.A. et al. Syndecan-1 Expression Is Associated with Tumor Size and EGFR Expression in Colorectal Carcinoma: a Clinicopathological Study of 230 Cases. Int J Med Sci 2015;12(2):92–9.
16. Shimada K., Anai S., Fujii T. et al. Syndecan-1 (CD138) contributes to prostate cancer progression by stabilizing tumourinitiating cells. J Pathol 2013;231(4): 495–504.
17. Zellweger T., Ninck C., Mirlacher M. et al. Tissue microarray analysis reveals prognostic significance of syndecan-1 expression in prostate cancer. Prostate 2003;55(1):20–9.
18. Xu Y., Yuan J., Zhang Z. et al. Syndecan-1 expression inhuman glioma is correlated with advanced tumor progression and poor prognosis. Mol Biol Rep 2012;39(9):8979–85.
19. Theocharis A.D., Skandalis S.S., Tzanakakis G., Karamanos N.K. Proteoglycans in health and disease: novel roles for proteoglycans in malignancy and their pharmacological targeting. FEBS J 2010;277(19):3904–23.
20. Iozzo R.V., Moscatello D.K., McQuillan D.J., Eichstetter I. Decorin is a biological ligand for the epidermal growth factor receptor. J Biol Chem 1999;274(8): 4489–92.
21. Merline R., Moreth K., Beckmann J. et al. Signaling by the matrix proteoglycan decorin controls inflammation and Cancer through PD CD4 and microRNA-21. Sci Signal 2011;4(199):ra75.
22. Albig A.R., Roy T., Becenti D.J., Schiemann W.P. Transcriptome analysis of endothelialcell gene expression induced by growth on matrigel matrices: identificationand characterization of MAGP-2 and lumican as novel regulators of angiogenesis. Angiogenesis 2007;10(3):197–216.
23. Matsuda Y., Yamamoto T., Kudo M. et al. Expression and roles of lumican in lung adenocarcinoma and squamous cell carcinoma. Int J Oncol 2008;33:1177–85.
24. Ishiwata T., Cho K., Kawahara K. et al. Role of lumican in cancer cells and adjacent stromal tissues in human pancreatic cancer. Onc Rep 2007;18(3):537–43.
25. Eshchenko T.Y., Rykova V.I., Chernakov A.E. et al. Expression of different proteoglycans in human breast tumors. Biochemistry (Mosc) 2007;72(9):1016–20.
26. Suhovskih A.V., Mostovich L.A., Kunin I.S. et al. Proteoglycan expression in normal human prostate tissue and prostate cancer. ISRN Oncol 2013;2013:680136.
27. Suhovskih A.V., Aidagulova S.V., Kashuba V.I., Grigorieva E.V. Proteoglycans as potential microenvironmental biomarkers for colon cancer. Cell Tissue Res 2015;361(3):833–44.
28. Skandalis S.S., Theocharis A.D., Theocharis D.A. et al. Matrix proteoglycans are markedly affected in advanced laryngeal squamous cell carcinoma. Biochim Biophys Acta 2004;1689(2):152–61.
29. Gulyás M., Hjerpe A. Proteoglycans and WT1 as markers for distinguishing adenocarcinoma, epithelioid mesothelioma, and benign mesothelium. J Pathol 2003;199(4):479–87.
30. García-Suárez O., García B., FernándezVega I. et al. Neuroendocrine tumors show altered expression of chondroitin sulfate, glypican 1, glypican 5, and syndecan 2 depending on their differentiation grade. Front Oncol 2014;4:15.
31. Nackaerts K., Verbeken E., Deneffe G. et al. Heparan sulfate proteoglycan expression in human lung-cancer cells. Int J Cancer 1997;74(3):335–45.
32. 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(2):259–70.
Review
For citations:
Suhovskih A.V., Grigor’eva E.V. Tissue-specificity of proteoglycans expression in different cancers. Advances in Molecular Oncology. 2016;3(1):53-60. (In Russ.) https://doi.org/10.17650/2313-805X.2016.3.1.53-60
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