Proteoglycans as potential microenvironmental biomarkers for colon cancer

Cell and Tissue Research

Volumn 361, Issue 3, 2015, Pages 833-844

  Suhovskih, Anastasia V ^a,b   Aidagulova, Svetlana V ^c   Kashuba, Vladimir I ^d,e   Grigorieva, Elvira V ^a,b,e  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOPHYSICS   (Russian Federation)

^b NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

^c NOVOSIBIRSK STATE MEDICAL UNIVERSITY   (Russian Federation)

^d INSTITUTE OF MOLECULAR BIOLOGY AND GENETICS   (Ukraine)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cancer biomarker; Colon cancer stem cell; Heparan sulfate biosynthesis; Microenvironment; Proteoglycan

Indexed keywords

AGGRECAN; BIGLYCAN; BIOLOGICAL MARKER; BREVICAN; COLLAGEN; COLLAGEN TYPE A1; CSPG4 PROTEIN; DECORIN; HERMES ANTIGEN; LUMICAN; MEMBRANE PROTEIN; PERLECAN; PROTEOGLYCAN; SERGLYCIN; SULF1 PROTEIN; SULF2 PROTEIN; SYNDECAN 1; UNCLASSIFIED DRUG; VERSICAN; PROTEOHEPARAN SULFATE;

ARTICLE; COLON CANCER; COLON CARCINOGENESIS; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE MARKER; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT; UPREGULATION; COLONIC NEOPLASMS; GENETICS; METABOLISM; PHYSIOLOGY;

BIGLYCAN; BIOMARKERS; COLONIC NEOPLASMS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; PROTEOGLYCANS; TUMOR MICROENVIRONMENT; UP-REGULATION; VERSICANS;

EID: 84940449931     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-015-2141-8     Document Type: Article

References (49)

1. Adany R, Iozzo RV (1990) Altered methylation of versican proteoglycan gene in human colon carcinoma. Biochem Biophys Res Commun 171:1402–1413
2. Adany R, Heimer R, Caterson B, Sorrell JM, Iozzo RV (1990) Altered expression of chondroitin sulfate proteoglycan in the stroma of human colon carcinoma. Hypomethylation of PG-40 gene correlates with increased PG-40 content and mRNA levels. J Biol Chem 265:11389–11396
3. Barbouri D, Afratis N, Gialeli C, Vynios DH, Theocharis AD, Karamanos NK (2014) Syndecans as modulators and potential pharmacological targets in cancer progression. Front Oncol 4:4, eCollection
4. Bi X, Tong C, Dockendorff A, Bancroft L, Gallagher L, Guzman G, Iozzo RV, Augenlicht LH, Yang W (2008) Genetic deficiency of decorin causes intestinal tumor formation through disruption of intestinal cell maturation. Carcinogenesis 29:1435–1440
5. Bi X, Pohl NM, Qian Z, Yang GR, Gou Y, Guzman G, Kajdacsy-Balla A, Iozzo RV, Yang W (2012) Decorin-mediated inhibition of colorectal cancer growth and migration is associated with E-cadherin in vitro and in mice. Carcinogenesis 33:326–330
6. Bret C, Moreaux J, Schved JF, Hose D, Klein B (2011) SULFs in human neoplasia: implication as progression and prognosis factors. J Transl Med 9:72
7. Chatzinikolaou G, Nikitovic D, Asimakopoulou A, Tsatsakis A, Karamanos NK, Tzanakakis GN (2008) Heparin–a unique stimulator of human colon cancer cells’ growth. IUBMB Life 60:333–340
8. Choi S, Kim Y, Park H, Han IO, Chung E, Lee SY, Kim YB, Lee JW, Oh ES, Yi JY (2009) Syndecan-2 overexpression regulates adhesion and migration through cooperation with integrin alpha2. Biochem Biophys Res Commun 384:231–235
9. Choi Y, Kim H, Chung H, Hwang JS, Shin JA, Han IO, Oh ES (2010) Syndecan-2 regulates cell migration in colon cancer cells through Tiam1-mediated Rac activation. Biochem Biophys Res Commun 391:921–925
10. Choi S, Kang DH, Oh ES (2013) Targeting syndecans: a promising strategy for the treatment of cancer. Expert Opin Ther Targets 17:695–705
11. Eshchenko TY, Rykova VI, Chernakov AE, Sidorov SV, Grigorieva EV (2007) Expression of different proteoglycans in human breast tumors. Biochemistry (Mosc) 72:1016–1020
12. Galamb O, Sipos F, Spisák S, Galamb B, Krenács T, Valcz G, Tulassay Z, Molnár B (2009) Potential biomarkers of colorectal adenoma-dysplasia-carcinoma progression: mRNA expression profiling and in situ protein detection on TMAs reveal 15 sequentially upregulated and 2 downregulated genes. Cell Oncol 31:19–29
13. García-Suárez O, García B, Fernández-Vega I, Astudillo A, Quirós LM (2014) Neuroendocrine tumors show altered expression of chondroitin sulfate, glypican 1, glypican 5, and syndecan 2 depending on their differentiation grade. Front Oncol 4:15. doi:10.3389/fonc.2014.00015. eCollection 2014
14. Gu X, Ma Y, Xiao J, Zheng H, Song C, Gong Y, Xing X (2012) Up-regulated biglycan expression correlates with the malignancy in human colorectal cancers. Clin Exp Med 12:195–199
15. Gulyás M, Hjerpe A (2003) Proteoglycans and WT1 as markers for distinguishing adenocarcinoma, epithelioid mesothelioma, and benign mesothelium. J Pathol 199:479–487
16. Hammond E, Khurana A, Shridhar V, Dredge K (2014) The role of heparanase and sulfatases in the modification of heparan sulfate proteoglycans within the tumor microenvironment and opportunities for novel cancer therapeutics. Front Oncol 4:195, eCollection
17. Haraguchi N, Ohkuma M, Sakashita H, Matsuzaki S, Tanaka F, Mimori K, Kamohara Y, Inoue H, Mori M (2008) CD133+ CD44+ population efficiently enriches colon cancer initiating cells. Ann Surg Oncol 15:2927–2933
18. Iozzo RV, Cohen I (1993) Altered proteoglycan gene expression and the tumor stroma. Experientia 49:447–455
19. Iozzo RV, Sanderson RD (2011) Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J Cell Mol Med 15:1013–1031
20. Joo EJ, Weyers A, Li G, Gasimli L, Li L, Choi WJ, Lee KB, Linhardt RJ (2014) Carbohydrate-containing molecules as potential biomarkers in colon cancer. OMICS 18:231–241
21. Kähäri VM, Larjava H, Uitto J (1991) Differential regulation of extracellular matrix proteoglycan (PG) gene expression. Transforming growth factor-beta 1 up-regulates biglycan (PGI), and versican (large fibroblast PG) but down-regulates decorin (PGII) mRNA levels in human fibroblasts in culture. J Biol Chem 266:10608–10615
22. Kinsella MG, Bressler SL, Wight TN (2004) The regulated synthesis of versican, decorin, and biglycan: extracellular matrix proteoglycans that influence cellular phenotype. Crit Rev Eukaryot Gene Expr 14:203–234
23. Knox S, Melrose J, Whitelock J (2001) Electrophoretic, biosensor, and bioactivity analyses of perlecans of different cellular origins. Proteomics 1:1534–1541
24. Kokenyesi R (2001) Ovarian carcinoma cells synthesize both chondroitin sulfate and heparan sulfate cell surface proteoglycans that mediate cell adhesion to interstitial matrix. J Cell Biochem 83:259–270
25. Kwon MJ, Kim Y, Choi Y, Kim SH, Park S, Han I, Kang DH, Oh ES (2013) The extracellular domain of syndecan-2 regulates the interaction of HCT116 human colon carcinoma cells with fibronectin. Biochem Biophys Res Commun 431:415–420
26. Lee H, Kim Y, Choi Y, Choi S, Hong E, Oh ES (2011) Syndecan-2 cytoplasmic domain regulates colon cancer cell migration via interaction with syntenin-1. Biochem Biophys Res Commun 409:148–153
27. Li YG, Ji DF, Zhong S, Zhu JX, Chen S, Hu GY (2011) Anti-tumor effects of proteoglycan from Phellinus linteus by immunomodulating and inhibiting Reg IV/EGFR/Akt signaling pathway in colorectal carcinoma. Int J Biol Macromol 48:511–517
28. Lundin M, Nordling S, Lundin J, Isola J, Wiksten JP, Haglund C (2005) Epithelial syndecan-1 expression is associated with stage and grade in colorectal cancer. Oncology 68:306–313
29. Mikula M, Rubel T, Karczmarski J, Goryca K, Dadlez M, Ostrowski J (2011) Integrating proteomic and transcriptomic high-throughput surveys for search of new biomarkers of colon tumors. Funct Integr Genomics 11:215–224
30. Molist A, Romarís M, Lindahl U, Villena J, Touab M, Bassols A (1998) Changes in glycosaminoglycan structure and composition of the main heparan sulphate proteoglycan from human colon carcinoma cells (perlecan) during cell differentiation. Eur J Biochem 254:371–377
31. Mukaratirwa S, Koninkx JF, Gruys E, Nederbragt H (2005) Mutual paracrine effects of colorectal tumour cells and stromal cells: modulation of tumour and stromal cell differentiation and extracellular matrix component production in culture. Int J Exp Pathol 86:219–229
32. Nackaerts K, Verbeken E, Deneffe G, Vanderschueren B, Demedts M, David G (1997) Heparan sulfate proteoglycan expression in human lung-cancer cells. Int J Cancer 74:335–345
33. Nikitovic D, Chatzinikolaou G, Tsiaoussis J, Tsatsakis A, Karamanos NK, Tzanakakis GN (2012) Insights into targeting colon cancer cell fate at the level of proteoglycans / glycosaminoglycans. Curr Med Chem 19:4247–4258
34. Pap Z, Pávai Z, Dénes L, Kovalszky I, Jung J (2009) An immunohistochemical study of colon adenomas and carcinomas: E-cadherin, Syndecan-1, Ets-1. Pathol Oncol Res 15:579–587
35. Pitule P, Vycital O, Bruha J, Novak P, Hosek P, Treska V, Hlavata I, Soucek P, Kralickova M, Liska V (2013) Differential expression and prognostic role of selected genes in colorectal cancer patients. Anticancer Res 33:4855–4865
36. Radwanska A, Litwin M, Nowak D, Baczynska D, Wegrowski Y, Maquart FX, Malicka-Blaszkiewicz M (2012) Overexpression of lumican affects the migration of human colon cancer cells through up-regulation of gelsolin and filamentous actin reorganization. Exp Cell Res 318:2312–2323
37. Ryu HY, Lee J, Yang S, Park H, Choi S, Jung KC, Lee ST, Seong JK, Han IO, Oh ES (2009) Syndecan-2 functions as a docking receptor for pro-matrix metalloproteinase-7 in human colon cancer cells. J Biol Chem 284:35692–35701
38. Sharma B, Handler M, Eichstetter I, Whitelock JM, Nugent MA, Iozzo RV (1998) Antisense targeting of perlecan blocks tumor growth and angiogenesis in vivo. J Clin Invest 102:1599–1608
39. Shimada K, Anai S, Fujii T, Tanaka N, Fujimoto K, Konishi N (2013) Syndecan-1 (CD138) contributes to prostate cancer progression by stabilizing tumour-initiating cells. J Pathol 231:495–504
40. Skandalis SS, Theocharis AD, Theocharis DA, Papadas T, Vynios DH, Papageorgakopoulou N (2004) Matrix proteoglycans are markedly affected in advanced laryngeal squamous cell carcinoma. Biochim Biophys Acta 1689:152–161
41. Suhovskih AV, Mostovich LA, Kunin IS, Boboev MM, Nepomnyashchikh GI, Aidagulova SV, Grigorieva EV (2013) Proteoglycan expression in normal human prostate tissue and prostate cancer. ISRN Oncol 2013:680136
42. Suhovskih AV, Tsidulko AY, Kutsenko OS, Kovner AV, Aidagulova SV, Ernberg I, Grigorieva EV (2014) Transcriptional activity of heparan sulfate biosynthetic machinery is specifically impaired in benign prostate hyperplasia and prostate cancer. Front Oncol 4:79, eCollection
43. Tallerico R, Todaro M, Di Franco S, Maccalli C, Garofalo C, Sottile R, Palmieri C, Tirinato L, Pangigadde PN, La Rocca R, Mandelboim O, Stassi G, Di Fabrizio E, Parmiani G, Moretta A, Dieli F, Kärre K, Carbone E (2013) Human NK cells selective targeting of colon cancer-initiating cells: a role for natural cytotoxicity receptors and MHC class I molecules. J Immunol 190:2381–2390
44. Tapanadechopone P, Tumova S, Jiang X, Couchman JR (2001) Epidermal transformation leads to increased perlecan synthesis with heparin-binding-growth-factor affinity. Biochem J 355:517–527
45. Theocharis AD (2002) Human colon adenocarcinoma is associated with specific post-translational modifications of versican and decorin. Biochim Biophys Acta 1588:165–172
46. Theocharis AD, Skandalis SS, Tzanakakis GN, Karamanos NK (2010) Proteoglycans in health and disease: novel roles for proteoglycans in malignancy and their pharmacological targeting. FEBS J 277:3904–3923
47. Vicente CM, Ricci R, Nader HB, Toma L (2013) Syndecan-2 is upregulated in colorectal cancer cells through interactions with extracellular matrix produced by stromal fibroblasts. BMC Cell Biol 14:25
48. Vivès RR, Seffouh A, Lortat-Jacob H (2014) Post-synthetic regulation of hs structure: the yin and yang of the sulfs in cancer. Front Oncol 3:331, eCollection
49. Yamamoto T, Eckes B, Krieg T (2001) Effect of interleukin-10 on the gene expression of type I collagen, fibronectin, and decorin in human skin fibroblasts: differential regulation by transforming growth factor-beta and monocyte chemoattractant protein-1. Biochem Biophys Res Commun 281:200–205