Versican 3′-untranslated region (3′-UTR) functions as a ceRNA in inducing the development of hepatocellular carcinoma by regulating miRNA activity

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 907-919

  Fang, Ling ^a,b   Du, William W ^a,b   Yang, Xiangling ^a,b   Chen, Kui ^d   Ghanekar, Anand ^b,d   Levy, Gary ^c   Yang, Weining ^a   Yee, Albert J ^a   Lu, Wei Yang ^e   Xuan, Jim W ^e   Gao, Zhongli ^f   Xie, Feng ^f   He, Chengyan ^f   Deng, Zhaoqun ^a,b   Yang, Burton B ^a,b  

^a Institute of Clinical Evaluative Sciences   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY HEALTH NETWORK   (Canada)

^e UNIVERSITY OF WESTERN ONTARIO   (Canada)

^f JILIN UNIVERSITY   (China)

Author keywords

MicroRNA; Noncoding RNA; Transgenic mice

Indexed keywords

CD34 ANTIGEN; FIBRONECTIN; MICRORNA; MICRORNA 133A; MICRORNA 144; MICRORNA 199A; MICRORNA 431; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VERSICAN; CSPG2 PROTEIN, MOUSE; ISOPROTEIN; RNA; TUMOR PROTEIN; VCAN PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL FUNCTION; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; COLONY FORMATION; CONTROLLED STUDY; GENETIC TRANSFECTION; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; CANCER INVASION; CELL STRAIN HEPG2; ENDOTHELIUM CELL; GENETICS; HUMAN; LIVER TUMOR; METABOLISM; METASTASIS; PATHOLOGY; TRANSGENIC MOUSE;

3' UNTRANSLATED REGIONS; ANIMALS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; ENDOTHELIAL CELLS; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MICE; MICE, TRANSGENIC; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; PROTEIN ISOFORMS; RNA, NEOPLASM; VERSICANS;

MLCS; MLOWN;

EID: 84874583945     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-220905     Document Type: Article

References (42)

1. Margolis, R. U., and Margolis, R. K. (1994) Aggrecan-versicanneurocan family proteoglycans. Methods Enzymol. 245, 105-126
2. Ito, K., Shinomura, T., Zako, M., Ujita, M., and Kimata, K. (1995) Multiple forms of mouse PG-M, a large chondroitin sulfate proteoglycan generated by alternative splicing. J. Biol. Chem. 270, 958-965
3. Brown, L. F., Guidi, A. J., Schnitt, S. J., Van De Water, L., Iruela-Arispe, M. L., Yeo, T. K., Tognazzi, K., and Dvorak, H. F. (1999) Vascular stroma formation in carcinoma in situ, invasive carcinoma, and metastatic carcinoma of the breast. Clin. Cancer Res. 5, 1041-1056 (Pubitemid 29233218)
4. Sheng, W., Wang, G., Wang, Y., Liang, J., Wen, J., Zheng, P. S., Wu, Y., Lee, V., Slingerland, J., Dumont, D., and Yang, B. B. (2005) The roles of versican V1 and V2 isoforms in cell proliferation and apoptosis. Mol. Biol. Cell 16, 1330-1340 (Pubitemid 40349568)
5. LaPierre, D. P., Lee, D. Y., Li, S. Z., Xie, Y. Z., Zhong, L., Sheng, W., Deng, Z., and Yang, B. B. (2007) The ability of versican to simultaneously cause apoptotic resistance and sensitivity. Cancer Res. 67, 4742-4750 (Pubitemid 46910181)
6. Lee, D. Y., Shatseva, T., Jeyapalan, Z., Du, W. W., Deng, Z., and Yang, B. B. (2009) A 3′-untranslated region (3=UTR) induces organ adhesion by regulating miR-199a* functions. PLoS One 4, e4527
7. Hutvagner, G., and Zamore, P. D. (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science 297, 2056-2060
8. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S., and Kim, V. N. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419 (Pubitemid 37187272)
9. Zeng, Y., and Cullen, B. R. (2004) Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. Nucleic Acids Res. 32, 4776-4785 (Pubitemid 39429682)
10. Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J., and Carthew, R. W. (2004) Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69-81 (Pubitemid 38469899)
11. Ye, W., Lv, Q., Wong, C. K., Hu, S., Fu, C., Hua, Z., Cai, G., Li, G., Yang, B. B., and Zhang, Y. (2008) The effect of central loops in miRNA: MRE duplexes on the efficiency of miRNA-mediated gene regulation. PLoS ONE 3, e1719
12. Lee, D. Y., Deng, Z., Wang, C. H., and Yang, B. B. (2007) MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proc. Natl. Acad. Sci. U. S. A. 104, 20350-20355
13. Yang, X., Rutnam, Z. J., Jiao, C., Wei, D., Xie, Y., Du, J., Zhong, L., and Yang, B. B. (2012) An anti-let-7 sponge decoys and decays endogenous let-7 functions. Cell Cycle 11, 3097-3108
14. Recchiuti, A., Krishnamoorthy, S., Fredman, G., Chiang, N., and Serhan, C. N. (2011) MicroRNAs in resolution of acute inflammation: identification of novel resolvin D1-miRNA circuits. FASEB J. 25, 544-560
15. Tarantino, C., Paolella, G., Cozzuto, L., Minopoli, G., Pastore, L., Parisi, S., and Russo, T. (2010) miRNA 34a, 100, and 137 modulate differentiation of mouse embryonic stem cells. FASEB J. 24, 3255-3263
16. Shan, S. W., Lee, D. Y., Deng, Z., Shatseva, T., Jeyapalan, Z., Du, W. W., Zhang, Y., Xuan, J. W., Yee, S. P., Siragam, V., and Yang, B. B. (2009) MicroRNA MiR-17 retards tissue growth and represses fibronectin expression. Nat. Cell Biol. 11, 1031-1038
17. Jeyapalan, Z., Deng, Z., Shatseva, T., Fang, L., He, C., and Yang, B. B. (2011) Expression of CD44 3′-untranslated region regulates endogenous microRNA functions in tumorigenesis and angiogenesis. Nucleic Acids Res. 39, 3026-3041
18. Lee, S. C., Fang, L., Wang, C. H., Kahai, S., Deng, Z., and Yang, B. B. (2011) A non-coding transcript of nephronectin promotes osteoblast differentiation by modulating microRNA functions. FEBS Lett. 585, 2610-2616
19. Rutnam, Z. J., and Yang, B. B. (2012) The non-coding 3= UTR of CD44 induces metastasis by regulating extracellular matrix functions. J. Cell Sci. 125, 2075-2085
20. Swami, M. (2010) Small RNAs: pseudogenes act as microRNA decoys. Nat. Rev. Cancer 10, 535
21. Poliseno, L., Salmena, L., Zhang, J., Carver, B., Haveman, W. J., and Pandolfi, P. P. (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465, 1033-1038
22. Cesana, M., Cacchiarelli, D., Legnini, I., Santini, T., Sthandier, O., Chinappi, M., Tramontano, A., and Bozzoni, I. (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147, 358-369
23. Seitz, H. (2009) Redefining microRNA targets. Curr. Biol. 19, 870-873
24. Kahai, S., Lee, S. C., Lee, D. Y., Yang, J., Li, M., Wang, C. H., Jiang, Z., Zhang, Y., Peng, C., and Yang, B. B. (2009) MicroRNA miR-378 regulates nephronectin expression modulating osteoblast differentiation by targeting GalNT-7. PLoS One 4, e7535
25. Zheng, P. S., Wen, J., Ang, L. C., Sheng, W., Viloria-Petit, A., Wang, Y., Wu, Y., Kerbel, R. S., and Yang, B. B. (2004) Versican/PG-M G3 domain promotes tumor growth and angiogenesis. FASEB J. 18, 754-756
26. Fang, L., Deng, Z., Shatseva, T., Yang, J., Peng, C., Du, W. W., Yee, A. J., Ang, L. C., He, C., Shan, S. W., and Yang, B. B. (2011) MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-beta8. Oncogene 30, 806-821
27. Shatseva, T., Lee, D. Y., Deng, Z., and Yang, B. B. (2011) MicroRNA miR-199a-3p regulates cell proliferation and survival by targeting caveolin-2. J. Cell Sci. 124, 2826-2836
28. Lin, H. M., Chatterjee, A., Lin, Y. H., Anjomshoaa, A., Fukuzawa, R., McCall, J. L., and Reeve, A. E. (2007) Genome wide expression profiling identifies genes associated with colorectal liver metastasis. Oncol. Rep. 17, 1541-1549
29. Setoguchi, T., Kikuchi, H., Yamamoto, M., Baba, M., Ohta, M., Kamiya, K., Tanaka, T., Baba, S., Goto-Inoue, N., Setou, M., Sasaki, T., Mori, H., Sugimura, H., and Konno, H. Microarray analysis identifies versican and CD9 as potent prognostic markers in gastric gastrointestinal stromal tumors. Cancer Sci. 102, 883-889
30. Yee, A. J., Akens, M., Yang, B. L., Finkelstein, J., Zheng, P. S., Deng, Z., and Yang, B. (2007) The effect of versican G3 domain on local breast cancer invasiveness and bony metastasis. Breast Cancer Res. 9, R47
31. Zimmermann, D. R., and Ruoslahti, E. (1989) Multiple domains of the large fibroblast proteoglycan, versican. EMBO J. 8, 2975-2981 (Pubitemid 19274999)
32. Sheng, W., Wang, G., La Pierre, D. P., Wen, J., Deng, Z., Wong, C. K., Lee, D. Y., and Yang, B. B. (2006) Versican mediates mesenchymal-epithelial transition. Mol. Biol. Cell. 17, 2009-2020 (Pubitemid 44011614)
33. Zheng, P. S., Vais, D., Lapierre, D., Liang, Y. Y., Lee, V., Yang, B. L., and Yang, B. B. (2004) PG-M/versican binds to P-selectin glycoprotein ligand-1 and mediates leukocyte aggregation. J. Cell Sci. 117, 5887-5895 (Pubitemid 40123954)
34. Arslan, F., Bosserhoff, A. K., Nickl-Jockschat, T., Doerfelt, A., Bogdahn, U., and Hau, P. (2007) The role of versican isoforms V0/V1 in glioma migration mediated by transforming growth factor-beta2. Br. J. Cancer 96, 1560-1568 (Pubitemid 46762960)
35. Shinomura, T., Nishida, Y., Ito, K., and Kimata, K. (1993) cDNA cloning of PG-M, a large chondroitin sulfate proteoglycan expressed during chondrogenesis in chick limb buds. Alternative spliced multiforms of PG-M and their relationships to versican. J. Biol. Chem. 268, 14461-14469 (Pubitemid 23195576)
36. Morita, H., Takeuchi, T., Suzuki, S., Maeda, K., Yamada, K., Eguchi, G., and Kimata, K. (1990) Aortic endothelial cells synthesize a large chondroitin sulphate proteoglycan capable of binding to hyaluronate. Biochem. J. 265, 61-68 (Pubitemid 20037674)
37. Miquel-Serra, L., Serra, M., Hernandez, D., Domenzain, C., Docampo, M. J., Rabanal, R. M., de Torres, I., Wight, T. N., Fabra, A., and Bassols, A. (2006) V3 versican isoform expression has a dual role in human melanoma tumor growth and metastasis. Lab. Invest. 86, 889-901 (Pubitemid 44268164)
38. Yamagata, M., Saga, S., Kato, M., Bernfield, M., and Kimata, K. (1993) Selective distributions of proteoglycans and their ligands in pericellular matrix of cultured fibroblasts. Implications for their roles in cell-substratum adhesion. J. Cell Sci. 106, 55-65 (Pubitemid 23286778)
39. Serra, M., Miquel, L., Domenzain, C., Docampo, M. J., Fabra, A., Wight, T. N., and Bassols, A. (2005) V3 versican isoform expression alters the phenotype of melanoma cells and their tumorigenic potential. Int. J. Cancer 114, 879-886
40. Lee, D. Y., Jeyapalan, Z., Fang, L., Yang, J., Zhang, Y., Yee, A. Y., Li, M., Du, W. W., Shatseva, T., and Yang, B. B. Expression of versican 3′-untranslated region modulates endogenous microRNA functions. PLoS One 5, e13599
41. Ricciardelli, C., Brooks, J. H., Suwiwat, S., Sakko, A. J., Mayne, K., Raymond, W. A., Seshadri, R., LeBaron, R. G., and Horsfall, D. J. (2002) Regulation of stromal versican expression by breast cancer cells and importance to relapse-free survival in patients with node-negative primary breast cancer. Clin. Cancer Res. 8, 1054-1060 (Pubitemid 35177355)
42. Schmalfeldt, M., Dours-Zimmermann, M. T., Winterhalter, K. H., and Zimmermann, D. R. (1998) Versican V2 is a major extracellular matrix component of the mature bovine brain. J. Biol. Chem. 273, 15758-15764 (Pubitemid 28298196)