Inhibition of fucosylation by 2-fluorofucose suppresses human liver cancer HepG2 cell proliferation and migration as well as tumor formation

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Zhou, Ying ^a   Fukuda, Tomohiko ^a   Hang, Qinglei ^a   Hou, Sicong ^a   Isaji, Tomoya ^a   Kameyama, Akihiko ^b   Gu, Jianguo ^a  

^a TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; FUCOSE; INTEGRIN; POLYSACCHARIDE;

CELL MOTION; CELL PROLIFERATION; CELL TRANSFORMATION; DRUG EFFECT; GLYCOSYLATION; HEP-G2 CELL LINE; HUMAN; INTRACELLULAR SPACE; METABOLISM; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; ERBB RECEPTORS; FUCOSE; GLYCOSYLATION; HEP G2 CELLS; HUMANS; INTEGRINS; INTRACELLULAR SPACE; POLYSACCHARIDES; SIGNAL TRANSDUCTION;

EID: 85029547224     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-11911-9     Document Type: Article

References (63)

1. Agard, N. J. & Bertozzi, C. R. Chemical approaches to perturb, profile, and perceive glycans. Acc Chem Res 42, 788-797, https://doi.org/10.1021/ar800267j (2009).
2. Kiessling, L. L. & Splain, R. A. Chemical approaches to glycobiology. Annu Rev Biochem 79, 619-653, https://doi.org/10.1146/annurev.biochem.77.070606.100917 (2010).
3. Miyoshi, E., et al. Fucosylation is a promising target for cancer diagnosis and therapy. Biomolecules 2, 34-45, https://doi.org/10.3390/biom2010034 (2012).
4. Vajaria, B. N. & Patel, P. S. Glycosylation: A hallmark of cancer Glycoconjugate journal 34, 147-156, https://doi.org/10.1007/s10719-016-9755-2 (2017).
5. Miyoshi, E., et al. The alpha1-6-fucosyltransferase gene and its biological significance. Biochim Biophys Acta 1473, 9-20 (1999).
6. Breborowicz, J., Mackiewicz, A. & Breborowicz, D. Microheterogeneity of alpha-fetoprotein in patient serum as demonstrated by lectin affino-electrophoresis. Scand J Immunol 14, 15-20 (1981).
7. Zhang, Y., et al. ESI-LC-MS Method for Haptoglobin Fucosylation Analysis in Hepatocellular Carcinoma and Liver Cirrhosis. Journal of proteome research 14, 5388-5395, https://doi.org/10.1021/acs.jproteome.5b00792 (2015).
8. Nie, H., et al. Specific N-glycans of Hepatocellular Carcinoma Cell Surface and the Abnormal Increase of Core-alpha-1, 6-fucosylated Triantennary Glycan via N-acetylglucosaminyltransferases-IVa Regulation. Sci Rep 5, 16007, https://doi.org/10.1038/srep16007 (2015).
9. Mehta, A., Herrera, H. & Block, T. Glycosylation and liver cancer. Advances in cancer research 126, 257-279, https://doi.org/10.1016/bs.acr.2014.11.005 (2015).
10. Yamashita, F., Tanaka, M., Satomura, S. & Tanikawa, K. Prognostic significance of Lens culinaris agglutinin A-reactive alpha-fetoprotein in small hepatocellular carcinomas. Gastroenterology 111, 996-1001 (1996).
11. Wang, Y., et al. Loss of alpha1, 6-fucosyltransferase suppressed liver regeneration: Implication of core fucose in the regulation of growth factor receptor-mediated cellular signaling. Sci Rep 5, 8264, https://doi.org/10.1038/srep08264 (2015).
12. Wang, Y., et al. Loss of alpha1, 6-fucosyltransferase inhibits chemical-induced hepatocellular carcinoma and tumorigenesis by down-regulating several cell signaling pathways. FASEB J 29, 3217-3227, https://doi.org/10.1096/fj.15-270710 (2015).
13. Tonetti, M., et al. The metabolism of 6-deoxyhexoses in bacterial and animal cells. Biochimie 80, 923-931 (1998).
14. Miyoshi, E., Moriwaki, K. & Nakagawa, T. Biological function of fucosylation in cancer biology. J Biochem 143, 725-729, https://doi.org/10.1093/jb/mvn011 (2008).
15. Tonetti, M., Sturla, L., Bisso, A., Benatti, U. & De Flora, A. Synthesis of GDP-L-fucose by the human FX protein. The Journal of biological chemistry 271, 27274-27279 (1996).
16. Ohyama, C., et al. Molecular cloning and expression of GDP-D-mannose-4, 6-dehydratase, a key enzyme for fucose metabolism defective in Lec13 cells. The Journal of biological chemistry 273, 14582-14587 (1998).
17. Sullivan, F. X., et al. Molecular cloning of human GDP-mannose 4, 6-dehydratase and reconstitution of GDP-fucose biosynthesis in vitro. The Journal of biological chemistry 273, 8193-8202 (1998).
18. Coffey, J. W., Miller, O. N. & Sellinger, O. Z. The Metabolism of L-Fucose in the Rat. The Journal of biological chemistry 239, 4011-4017 (1964).
19. Kaufman, R. L. & Ginsburg, V. The metabolism of L-fucose by HeLa cells. Exp Cell Res 50, 127-132 (1968).
20. Becker, D. J. & Lowe, J. B. Fucose: Biosynthesis and biological function in mammals. Glycobiology 13, 41R-53R, https://doi.org/10.1093/glycob/cwg054 (2003).
21. Nakayama, K., et al. Mutation of GDP-mannose-4, 6-dehydratase in colorectal cancer metastasis. PLoS One 8, e70298, https://doi.org/10.1371/journal.pone.0070298 (2013).
22. Louie, S., et al. FX knockout CHO hosts can express desired ratios of fucosylated or afucosylated antibodies with high titers and comparable product quality. Biotechnol Bioeng 114, 632-644, https://doi.org/10.1002/bit.26188 (2017).
23. Moriwaki, K., et al. Deficiency of GMDS leads to escape from NK cell-mediated tumor surveillance through modulation of TRAIL signaling. Gastroenterology 137(188-198), 198 e181-182, https://doi.org/10.1053/j.gastro.2009.04.002 (2009).
24. Moriwaki, K., Shinzaki, S. & Miyoshi, E. GDP-mannose-4, 6-dehydratase (GMDS) deficiency renders colon cancer cells resistant to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) receptor-and CD95-mediated apoptosis by inhibiting complex II formation. The Journal of biological chemistry 286, 43123-43133, https://doi.org/10.1074/jbc.M111.262741 (2011).
25. Sturla, L., et al. Impairment of the Golgi GDP-L-fucose transport and unresponsiveness to fucose replacement therapy in LAD II patients. Pediatr Res 49, 537-542, https://doi.org/10.1203/00006450-200104000-00016 (2001).
26. Gloster, T. M. & Vocadlo, D. J. Developing inhibitors of glycan processing enzymes as tools for enabling glycobiology. Nature chemical biology 8, 683-694, https://doi.org/10.1038/nchembio.1029 (2012).
27. Manabe, Y., et al. Development of alpha1, 6-fucosyltransferase inhibitors through the diversity-oriented syntheses of GDP-fucose mimics using the coupling between alkyne and sulfonyl azide. Bioorganic & medicinal chemistry 25, 2844-2850, https://doi.org/10.1016/j.bmc.2017.02.036 (2017).
28. Tu, Z., Lin, Y. N. & Lin, C. H. Development of fucosyltransferase and fucosidase inhibitors. Chemical Society reviews 42, 4459-4475, https://doi.org/10.1039/c3cs60056d (2013).
29. Rillahan, C. D., et al. Global metabolic inhibitors of sialyl-and fucosyltransferases remodel the glycome. Nature chemical biology 8, 661-668, https://doi.org/10.1038/nchembio.999 (2012).
30. Okeley, N. M., et al. Development of orally active inhibitors of protein and cellular fucosylation. Proc Natl Acad Sci USA 110, 5404-5409, https://doi.org/10.1073/pnas.1222263110 (2013).
31. Belcher, J. D., et al. The fucosylation inhibitor, 2-fluorofucose, inhibits vaso-occlusion, leukocyte-endothelium interactions and NF-kB activation in transgenic sickle mice. PLoS One 10, e0117772, https://doi.org/10.1371/journal.pone.0117772 (2015).
32. Villalobos, J. A., Yi, B. R. & Wallace, I. S. 2-Fluoro-L-Fucose Is a Metabolically Incorporated Inhibitor of Plant Cell Wall Polysaccharide Fucosylation. PLoS One 10, e0139091, https://doi.org/10.1371/journal.pone.0139091 (2015).
33. Dumont, M., et al. Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy-L-fucose induces defects in root cell elongation. Plant J 84, 1137-1151, https://doi.org/10.1111/tpj.13071 (2015).
34. Matsumura, K., et al. Carbohydrate binding specificity of a fucose-specific lectin from Aspergillus oryzae: A novel probe for core fucose. The Journal of biological chemistry 282, 15700-15708, https://doi.org/10.1074/jbc.M701195200 (2007).
35. Cheng, L., et al. Comprehensive N-glycan profiles of hepatocellular carcinoma reveal association of fucosylation with tumor progression and regulation of FUT8 by microRNAs. Oncotarget 7, 61199-61214, https://doi.org/10.18632/oncotarget.11284 (2016).
36. Chen, L. L., et al. Retroviral gene transfer of epidermal growth factor receptor into HL60 cells results in a partial block of retinoic acid-induced granulocytic differentiation. Cell growth & differentiation: The molecular biology journal of the American Association for Cancer Research 4, 769-776 (1993).
37. Jo, M., Thomas, K. S., O'Donnell, D. M. & Gonias, S. L. Epidermal growth factor receptor-dependent and-independent cell-signaling pathways originating from the urokinase receptor. The Journal of biological chemistry 278, 1642-1646, https://doi.org/10.1074/jbc.M210877200 (2003).
38. Li, Y. M., et al. Regulation of myeloid growth and differentiation by the insulin-like growth factor I receptor. Endocrinology 138, 362-368, https://doi.org/10.1210/endo.138.1.4847 (1997).
39. Sinclair, J., McClain, D. & Taetle, R. Effects of insulin and insulin-like growth factor I on growth of human leukemia cells in serum-free and protein-free medium. Blood 72, 66-72 (1988).
40. Lau, K. S., et al. Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell 129, 123-134, https://doi.org/10.1016/j.cell.2007.01.049 (2007).
41. Fernandes, H., Cohen, S. & Bishayee, S. Glycosylation-induced conformational modification positively regulates receptor-receptor association: A study with an aberrant epidermal growth factor receptor (EGFRvIII/DeltaEGFR) expressed in cancer cells. The Journal of biological chemistry 276, 5375-5383, https://doi.org/10.1074/jbc.M005599200 (2001).
42. Zhao, Y., et al. Deletion of core fucosylation on alpha3beta1 integrin down-regulates its functions. The Journal of biological chemistry 281, 38343-38350, https://doi.org/10.1074/jbc.M608764200 (2006).
43. Kobayashi, Y., et al. A novel core fucose-specific lectin from the mushroom Pholiota squarrosa. The Journal of biological chemistry 287, 33973-33982, https://doi.org/10.1074/jbc.M111.327692 (2012).
44. Bosch, F. X., Ribes, J. & Borras, J. Epidemiology of primary liver cancer. Seminars in liver disease 19, 271-285, https://doi.org/10.1055/s-2007-1007117 (1999).
45. Sia, D., Villanueva, A., Friedman, S. L. & Llovet, J. M. Liver Cancer Cell of Origin, Molecular Class, and Effects on Patient Prognosis. Gastroenterology, doi: Https://doi.org/10.1053/j.gastro.2016.11.048 (2016).
46. Noro, E., et al. Large-Scale Identification of N-Glycan Glycoproteins Carrying Lewis x and Site-Specific N-Glycan Alterations in Fut9 Knockout Mice. Journal of proteome research 14, 3823-3834, https://doi.org/10.1021/acs.jproteome.5b00178 (2015).
47. Vajaria, B. N. & Patel, P. S. Glycosylation: A hallmark of cancer Glycoconjugate journal, doi: Https://doi.org/10.1007/s10719-016-9755-2 (2016).
48. Padler-Karavani, V. Aiming at the sweet side of cancer: Aberrant glycosylation as possible target for personalized-medicine. Cancer Lett 352, 102-112, https://doi.org/10.1016/j.canlet.2013.10.005 (2014).
49. Reis, C. A., Osorio, H., Silva, L., Gomes, C. & David, L. Alterations in glycosylation as biomarkers for cancer detection. J Clin Pathol 63, 322-329, https://doi.org/10.1136/jcp.2009.071035 (2010).
50. Wang, X., et al. Core fucosylation regulates epidermal growth factor receptor-mediated intracellular signaling. The Journal of biological chemistry 281, 2572-2577, https://doi.org/10.1074/jbc.M510893200 (2006).
51. Liu, Y. C., et al. Sialylation and fucosylation of epidermal growth factor receptor suppress its dimerization and activation in lung cancer cells. Proc Natl Acad Sci USA 108, 11332-11337, https://doi.org/10.1073/pnas.1107385108 (2011).
52. Kaszuba, K., et al. N-Glycosylation as determinant of epidermal growth factor receptor conformation in membranes. Proc Natl Acad Sci USA 112, 4334-4339, https://doi.org/10.1073/pnas.1503262112 (2015).
53. Schwartz, M. A. & Ginsberg, M. H. Networks and crosstalk: Integrin signalling spreads. Nature cell biology 4, E65-68, https://doi.org/10.1038/ncb0402-e65 (2002).
54. Cabodi, S., et al. Integrin regulation of epidermal growth factor (EGF) receptor and of EGF-dependent responses. Biochemical Society transactions 32, 438-442, https://doi.org/10.1042/BST0320438 (2004).
55. Guo, H. B., Lee, I., Kamar, M., Akiyama, S. K. & Pierce, M. Aberrant N-glycosylation of beta1 integrin causes reduced alpha5beta1 integrin clustering and stimulates cell migration. Cancer research 62, 6837-6845 (2002).
56. Seales, E. C., et al. Hypersialylation of beta1 integrins, observed in colon adenocarcinoma, may contribute to cancer progression by up-regulating cell motility. Cancer research 65, 4645-4652, https://doi.org/10.1158/0008-5472.CAN-04-3117 (2005).
57. Isaji, T., et al. Introduction of bisecting GlcNAc into integrin alpha5beta1 reduces ligand binding and down-regulates cell adhesion and cell migration. The Journal of biological chemistry 279, 19747-19754, https://doi.org/10.1074/jbc.M311627200 (2004).
58. Hou, S., et al. Distinct effects of beta1 integrin on cell proliferation and cellular signaling in MDA-MB-231 breast cancer cells. Sci Rep 6, 18430, https://doi.org/10.1038/srep18430 (2016).
59. Sieg, D. J., et al. FAK integrates growth-factor and integrin signals to promote cell migration. Nature cell biology 2, 249-256, https://doi.org/10.1038/35010517 (2000).
60. Mitra, S. K. & Schlaepfer, D. D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Current opinion in cell biology 18, 516-523, https://doi.org/10.1016/j.ceb.2006.08.011 (2006).
61. Schultz, M. J., Swindall, A. F. & Bellis, S. L. Regulation of the metastatic cell phenotype by sialylated glycans. Cancer metastasis reviews 31, 501-518, https://doi.org/10.1007/s10555-012-9359-7 (2012).
62. Lu, J. & Gu, J. Significance of beta-Galactoside alpha2, 6 Sialyltranferase 1 in Cancers. Molecules 20, 7509-7527, https://doi.org/10.3390/molecules20057509 (2015).
63. Dong, W., Matsuno, Y. K. & Kameyama, A. A procedure for Alcian blue staining of mucins on polyvinylidene difluoride membranes. Anal Chem 84, 8461-8466, https://doi.org/10.1021/ac301678z (2012).