Silencing of hHS6ST2 inhibits progression of pancreatic cancer through inhibition of Notch signalling

Biochemical Journal

Volumn 436, Issue 2, 2011, Pages 271-282

  Song, Kai ^a   Li, Qin ^a   Peng, Yong Bo ^a   Li, Jie ^b   Ding, Kan ^b   Chen, Li Juan ^c   Shao, Cheng Hao ^d   Zhang, Li Jun ^e   Li, Ping ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^c SICHUAN UNIVERSITY   (China)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

^e SHANGHAI PUBLIC HEALTH CLINICAL CENTER   (China)

Author keywords

6 O sulfotransferase; Angiogenesis; Epithelial mesenchymal transition (EMT); Heparan sulfate; Notch; Pancreatic cancer; Proteomics

Indexed keywords

HEPARAN SULFATE; HEPARAN SULFATE DEXTRO GLUCOSAMINYL 6 O SULFOTRANSFERASE 2; NOTCH RECEPTOR; SHORT HAIRPIN RNA; SULFOTRANSFERASE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS CANCER; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SULFATION; TUMOR CELL; UPREGULATION;

ANIMALS; CELL LINE; CELL LINE, TUMOR; DISEASE PROGRESSION; DOWN-REGULATION; ENDOTHELIAL CELLS; FEMALE; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; PANCREATIC NEOPLASMS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; SULFOTRANSFERASES;

MUS;

EID: 79956050747     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110297     Document Type: Article

References (35)

1. Bernfield, M., Gotte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J. and Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777
2. Esko, J. D. and Lindahl, U. (2001) Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169-173
3. Ashikari-Hada, S., Habuchi, H., Kariya, Y., Itoh, N., Reddi, A. H. and Kimata, K. (2004) Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J. Biol. Chem. 279, 12346-12354
4. Kamimura, K., Fujise, M., Villa, F., Izumi, S., Habuchi, H., Kimata, K. and Nakato, H. (2001) Drosophila heparan sulfate 6-O-sulfotransferase (dHS6ST ) gene: structure, expression, and function in the formation of the tracheal system. J. Biol. Chem. 276, 17014-17021
5. Bulow, H. E. and Hobert, O. (2004) Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron 41, 723-736 (Pubitemid 38326835)
6. Bink, R. J., Habuchi, H., Lele, Z., Dolk, E., Joore, J., Rauch, G. J., Geisler, R., Wilson, S. W., den Hertog, J., Kimata, K. and Zivkovic, D. (2003) Heparan sulfate 6-O-sulfotransferase is essential for muscle development in zebrafish. J. Biol. Chem. 278, 31118-31127
7. Chen, E., Stringer, S. E., Rusch, M. A., Selleck, S. B. and Ekker, S. C. (2005) A unique role for 6-O sulfation modification in zebrafish vascular development. Dev. Biol. 284, 364-376
8. Irie, A., Yates, E. A., Turnbull, J. E. and Holt, C. E. (2002) Specific heparan sulfate structures involved in retinal axon targeting. Development 129, 61-70
9. Habuchi, H., Nagai, N., Sugaya, N., Atsumi, F., Stevens, R. L. and Kimata, K. (2007) Mice deficient in heparan sulfate 6-O-sulfotransferase-1 exhibit defective heparan sulfate biosynthesis, abnormal placentation, and late embryonic lethality. J. Biol. Chem. 282, 15578-15588
10. Grego-Bessa, J., Diez, J., Timmerman, L. and de la Pompa, J. L. (2004) Notch and epithelial-mesenchyme transition in development and tumor progression: another turn of the screw. Cell Cycle 3, 718-721
11. Miyamoto, Y., Maitra, A., Ghosh, B., Zechner, U., Argani, P., Iacobuzio-Donahue, C. A., Sriuranpong, V., Iso, T., Meszoely, I. M., Wolfe, M. S. et al. (2003) Notch mediates TGFα-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell 3, 565-576 (Pubitemid 36808651)
12. Sahlgren, C., Gustafsson, M. V., Jin, S., Poellinger, L. and Lendahl, U. (2008) Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc. Natl. Acad. Sci. U.S.A. 105, 6392-6397
13. Gridley, T. (2007) Notch signaling in vascular development and physiology. Development 134, 2709-2718
14. Noguera-Troise, I., Daly, C., Papadopoulos, N. J., Coetzee, S., Boland, P., Gale, N. W., Lin, H. C., Yancopoulos, G. D. and Thurston, G. (2006) Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444, 1032-1037 (Pubitemid 46018516)
15. Haines, N. and Irvine, K. D. (2003) Glycosylation regulates Notch signalling. Nat. Rev. Mol. Cell Biol. 4, 786-797
16. Habuchi, H., Miyake, G., Nogami, K., Kuroiwa, A., Matsuda, Y., Kusche-Gullberg, M., Habuchi, O., Tanaka, M. and Kimata, K. (2003) Biosynthesis of heparan sulphate with diverse structures and functions: two alternatively spliced forms of human heparan sulphate 6-O-sulphotransferase-2 having different expression patterns and properties. Biochem. J. 371, 131-142 (Pubitemid 36458087)
17. Seko, A., Kataoka, F., Aoki, D., Sakamoto, M., Nakamura, T., Hatae, M., Yonezawa, S. and Yamashita, K. (2009) N-Acetylglucosamine 6-O-sulfotransferase-2 as a tumor marker for uterine cervical and corpus cancer. Glycoconjugate J. 26, 1065-1073
18. Lundin, L., Larsson, H., Kreuger, J., Kanda, S., Lindahl, U., Salmivirta, M. and Claesson-Welsh, L. (2000) Selectively desulfated heparin inhibits fibroblast growth factor-induced mitogenicity and angiogenesis. J. Biol. Chem. 275, 24653-24660
19. Karantza, V. (2011) Keratins in health and cancer: more than mere epithelial cell markers. Oncogene 30, 127-138
20. Leong, K. G., Niessen, K., Kulic, I., Raouf, A., Eaves, C., Pollet, I. and Karsan, A. (2007) Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin. J. Exp. Med. 204, 2935-2948
21. Wang, Z., Li, Y., Kong, D., Banerjee, S., Ahmad, A., Azmi, A. S., Ali, S., Abbruzzese, J. L., Gallick, G. E. and Sarkar, F. H. (2009) Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res. 69, 2400-2407
22. Choi, H. S., Yim, S. H., Xu, H. D., Jung, S. H., Shin, S. H., Hu, H. J., Jung, C. K., Choi, J. Y. and Chung, Y. J. (2010) Tropomyosin3 overexpression and a potential link to epithelial-mesenchymal transition in human hepatocellular carcinoma. BMC Cancer 10, 122
23. Tauler, J., Zudaire, E., Liu, H., Shih, J. and Mulshine, J. L. (2010) hnRNP A2/B1 modulates epithelial-mesenchymal transition in lung cancer cell lines. Cancer Res. 70, 7137-7147
24. Yoo, H. J., Yun, B. R., Kwon, J. H., Ahn, H. S., Seol, M. A., Lee, M. J., Yu, G. R., Yu, H. C., Hong, B., Choi, K. and Kim, D. G. (2009) Genetic and expression alterations in association with the sarcomatous change of cholangiocarcinoma cells. Exp. Mol. Med. 41, 102-115
25. Maschler, S., Gebeshuber, C. A., Wiedemann, E. M., Alacakaptan, M., Schreiber, M., Custic, I. and Beug, H. (2010) Annexin A1 attenuates EMT and metastatic potential in breast cancer. EMBO Mol. Med. 2, 401-414
26. Keshamouni, V. G., Jagtap, P., Michailidis, G., Strahler, J. R., Kuick, R., Reka, A. K., Papoulias, P., Krishnapuram, R., Srirangam, A., Standiford, T. J. et al. (2009) Temporal quantitative proteomics by iTRAQ 2D-LC-MS/MS and corresponding mRNA expression analysis identify post-transcriptional modulation of actin-cytoskeleton regulators during TGF-β-induced epithelial- mesenchymal transition. J. Proteome Res. 8, 35-47
27. Kobayashi, M., Sugiyama, H., Wang, D. H., Toda, N., Maeshima, Y., Yamasaki, Y., Masuoka, N., Yamada, M., Kira, S. and Makino, H. (2005) Catalase deficiency renders remnant kidneys more susceptible to oxidant tissue injury and renal fibrosis in mice. Kidney Int. 68, 1018-1031 (Pubitemid 43246418)
28. Tanaka, K., Tanaka, Y., Namba, T., Azuma, A. and Mizushima, T. (2010) Heat shock protein 70 protects against bleomycin-induced pulmonary fibrosis in mice. Biochem. Pharmacol. 80, 920-931
29. Ali-Fehmi, R., Chatterjee, M., Ionan, A., Levin, N. K., Arabi, H., Bandyopadhyay, S., Shah, J. P., Bryant, C. S., Hewitt, S. M., O'Rand, M. G. et al. (2010) Analysis of the expression of human tumor antigens in ovarian cancer tissues. Cancer Biomarkers 6, 33-48
30. Demir, A. Y., Groothuis, P. G., Dunselman, G. A., Schurgers, L., Evers, J. L. and de Goeij, A. F. (2005) Molecular characterization of soluble factors from human menstrual effluent that induce epithelial to mesenchymal transitions in mesothelial cells. Cell Tissue Res. 322, 299-311
31. Yang, J. H., Wylie-Sears, J. and Bischoff, J. (2008) Opposing actions of Notch1 and VEGF in post-natal cardiac valve endothelial cells. Biochem. Biophys. Res. Commun. 374, 512-516
32. Niessen, K., Fu, Y., Chang, L., Hoodless, P. A., McFadden, D. and Karsan, A. (2008) Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J. Cell Biol. 182, 315-325
33. Siekmann, A. F. and Lawson, N. D. (2007) Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784
34. Yamanda, S., Ebihara, S., Asada, M., Okazaki, T., Niu, K., Ebihara, T., Koyanagi, A., Yamaguchi, N., Yagita, H. and Arai, H. (2009) Role of ephrinB2 in nonproductive angiogenesis induced by Delta-like 4 blockade. Blood 113, 3631-3639
35. Kamimura, K., Rhodes, J. M., Ueda, R., McNeely, M., Shukla, D., Kimata, K., Spear, P. G., Shworak, N. W. and Nakato, H. (2004) Regulation of Notch signaling by Drosophila heparan sulfate 3-O sulfotransferase. J. Cell Biol. 166, 1069-1079