Bioengineered chinese hamster ovary cells with golgi-targeted 3-O-sulfotransferase-1 biosynthesize heparan sulfate with an antithrombin-binding site

Journal of Biological Chemistry

Volumn 288, Issue 52, 2013, Pages 37308-37318

  Datta, Payel ^a,b   Li, Guoyun ^b,c,d   Yang, Bo ^b,c   Zhao, Xue ^d   Baik, Jong Youn ^e   Gemmill, Trent R ^e   Sharfstein, Susan T ^e   Linhardt, Robert J ^a,b,c  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b Rensselaer Polytechnic Institute   (United States)

^c RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^d OCEAN UNIVERSITY OF CHINA   (China)

^e SUNY POLYTECHNIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-COAGULANT DRUGS; BIOSYNTHETIC ENZYMES; CHINESE HAMSTER OVARY CELLS; HEPARAN SULFATES;

BIOCHEMISTRY;

BIOSYNTHESIS;

DISACCHARIDE; HEPARAN SULFATE; HEPARAN SULFATE 3 O SULFOTRANSFERASE ISOFORM 1; HISTONE DEACETYLASE; N DEACETYLASE ISOFORM 2; N SULFOTRANSFERASE ISOFORM 2; SULFOTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; BIOSYNTHESIS; CELL ENGINEERING; CHO CELL; CONTROLLED STUDY; ENZYME LOCALIZATION; FEMALE; GENE OVEREXPRESSION; GOLGI COMPLEX; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; UPREGULATION;

EID: 84891383477     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.519033     Document Type: Article

References (54)

1. Dreyfuss, J. L., Regatieri, C. V., Jarrouge, T. R., Cavalheiro, R. P., Sampaio, L. O., and Nader, H. B. (2009) Heparan sulfate proteoglycans: structure, protein interactions and cell signaling. An. Academ. Bras. Cienc. 81, 409-429
2. Liu, H., Zhang, Z., and Linhardt, R. J. (2009) Lessons learned from the contamination of heparin. Nat. Prod. Rep. 26, 313-321
3. Carlsson, P., and Kjellén, L. (2012) Heparin biosynthesis. Handb. Exp. Pharmacol. 207, 23-41
4. Esko, J. D., and Lindahl, U. (2001) Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169-173
5. Esko, J. D., and Zhang, L. (1996) Influence of core protein sequence on glycosaminoglycan assembly. Curr. Opin. Struct. Biol. 6, 663-670
6. Gulberti, S., Lattard, V., Fondeur, M., Jacquinet, J. C., Mulliert, G., Netter, P., Magdalou, J., Ouzzine, M., and Fournel-Gigleux, S. (2005) Phosphorylation and sulfation of oligosaccharide substrates critically influence the activity of human β1,4-galactosyltransferase 7 (GalT-I) and β1,3-glucuronosyltransferase I (GlcAT-I) involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans. J. Biol. Chem. 280, 1417-1425
7. Tone, Y., Pedersen, L. C., Yamamoto, T., Izumikawa, T., Kitagawa, H., Nishihara, J., Tamura, J., Negishi, M., and Sugahara, K. (2008) 2-O-Phosphorylation of xylose and 6-O-sulfation of galactose in the protein linkage region of glycosaminoglycans influence the glucuronyltransferase-I activity involved in the linkage region synthesis. J. Biol. Chem. 283, 16801-16807
8. Duelli, A., Rönnberg, E., Waern, I., Ringvall, M., Kolset, S. O., and Pejler, G. (2009) Mast cell differentiation and activation is closely linked to expression of genes coding for the serglycin proteoglycan core protein and a distinct set of chondroitin sulfate and heparin sulfotransferases. J. Immunol. 183, 7073-7083
9. Kramer, K. L., and Yost, H. J. (2003) Heparan sulfate core proteins in cell-cell signaling. Annu. Rev. Genet. 37, 461-484
10. Wang, Z., Ly, M., Zhang, F., Zhong, W., Suen, A., Hickey, A. M., Dordick, J. S., and Linhardt, R. J. (2010) E. coli K5 fermentation and the preparation of heparosan, a bioengineered heparin precursor. Biotechnol. Bioeng. 107, 964-973
11. Grobe, K., Ledin, J., Ringvall, M., Holmborn, K., Forsberg, E., Esko, J. D., and Kjellén, L. (2002) Heparan sulfate and development: differential roles of the N-acetylglucosamine N-deacetylase/N-sulfotransferase isozymes. Biochim. Biophys. Acta 1573, 209-215
12. Hashimoto, Y., Orellana, A., Gil, G., and Hirschberg, C. B. (1992) Molecular cloning and expression of rat liverN-heparan sulfate sulfotransferase. J. Biol. Chem. 267, 15744-15750
13. Aikawa, J., and Esko, J. D. (1999) Molecular cloning and expression of a third member of the heparan sulfate/heparin GlcNAc N-deacetylase/ Nsulfotransferase family. J. Biol. Chem. 274, 2690-2695
14. Aikawa, J., Grobe, K., Tsujimoto, M., and Esko, J. D. (2001) Multiple isozymes of heparan sulfate/heparin GlcNAc N-deacetylase/GlcN N-sulfotransferase. Structure and activity of the fourth member, NDST4. J. Biol. Chem. 276, 5876-5882
15. Eriksson, I., Sandbäck, D., Ek, B., Lindahl, U., and Kjellén, L. (1994) cDNA cloning and sequencing of mouse mastocytoma glucosaminyl N-deacetylase/N-sulfotransferase, an enzyme involved in the biosynthesis of heparin. J. Biol. Chem. 269, 10438-10443
16. Kusche-Gullberg, M., Eriksson, I., Pikas, D. S., and Kjellén, L. (1998) Identification and expression in mouse of two heparan sulfate glucosaminyl N-deacetylase/N-sulfotransferase genes. J. Biol. Chem. 273, 11902-11907
17. Orellana, A., Hirschberg, C. B., Wei, Z., Swiedler, S. J., and Ishihara, M. (1994) Molecular cloning and expression of a glycosaminoglycan N-acetylglucosaminyl N-deacetylase/N-sulfotransferase from a heparinproducing cell line. J. Biol. Chem. 269, 2270-2276
18. Cheung, W. F., Eriksson, I., Kusche-Gullberg, M., Lindhal, U., and Kjellén, L. (1996) Expression of the mouse mastocytoma glucosaminyl N-deacetylase/N-sulfotransferase in human kidney 293 cells results in increased N-sulfation of heparan sulfate. Biochemistry 35, 5250-5256
19. Jacobsson, I., Lindahl, U., Jensen, J. W., Rodén, L., Prihar, H., and Feingold, D. S. (1984) Biosynthesis of heparin. Substrate specificity of heparosan N-sulfate D-glucuronosyl 5-epimerase. J. Biol. Chem. 259, 1056-1063
20. Rong, J., Habuchi, H., Kimata, K., Lindahl, U., and Kusche-Gullberg, M. (2001) Substrate specificity of the heparan sulfate hexuronic acid 2-Osulfotransferase, Biochemistry 40, 5548-5555
21. 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
22. Habuchi, H., Tanaka, M., Habuchi, O., Yoshida, K., Suzuki, H., Ban, K., and Kimata, K. (2000) The occurrence of three isoforms of heparan sulfate 6-O-sulfotransferase having different specificities for hexuronic acid adjacent to the targeted N-sulfoglucosamine. J. Biol. Chem. 275, 2859-2868
23. Jemth, P., Smeds, E., Do, A. T., Habuchi, H., Kimata, K., Lindahl, U., and Kusche-Gullberg, M. (2003) Oligosaccharide library-based assessment of heparan sulfate 6-O-sulfotransferase substrate specificity. J. Biol. Chem. 278, 24371-24376
24. Smeds, E., Habuchi, H., Do, A. T., Hjertson, E., Grundberg, H., Kimata, K., Lindahl, U., and Kusche-Gullberg, M. (2003) Substrate specificities of mouse heparan sulphate glucosaminyl 6-O-sulphotransferases. Biochem. J. 372, 371-380
25. Girardin, E. P., Hajmohammadi, S., Birmele, B., Helisch, A., Shworak, N. W., and de Agostini, A. I. (2005) Synthesis of anticoagulantly active heparan sulfate proteoglycans by glomerular epithelial cells involves multiple 3-O-sulfotransferase isoforms and a limiting precursor pool. J. Biol. Chem. 280, 38059-38070
26. Liu, J., Shworak, N. W., Sinaÿ, P., Schwartz, J. J., Zhang, L., Fritze, L. M., and Rosenberg, R. D. (1999) Expression of heparan sulfate D-glucosaminyl 3-O-sulfotransferase isoforms reveals novel substrate specificities. J. Biol. Chem. 274, 5185-5192
27. Shworak, N. W., Liu, J., Petros, L. M., Zhang, L., Kobayashi, M., Copeland, N. G., Jenkins, N. A., and Rosenberg, R. D. (1999) Multiple isoforms of heparan sulfate D-glucosaminyl 3-O-sulfotransferase. Isolation, characterization, and expression of human cDNAs and identification of distinct genomic loci. J. Biol. Chem. 274, 5170-5184
28. Esko, J. D., and Selleck, S. B. (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-471
29. Humphries, D. E., Wong, G. W., Friend, D. S., Gurish, M. F., Qiu, W. T., Huang, C., Sharpe, A. H., and Stevens, R. L. (1999) Heparin is essential for the storage of specific granule proteases in mast cells. Nature 400, 769-772
30. Forsberg, E., Pejler, G., Ringvall, M., Lunderius, C., Tomasini-Johansson, B., Kusche-Gullberg, M., Eriksson, I., Ledin, J., Hellman, L., and Kjellén, L. (1999) Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature 400, 773-776
31. Feyerabend, T. B., Li, J. P., Lindahl, U., and Rodewald, H. R. (2006) Heparan sulfate C5-epimerase is essential for heparin biosynthesis in mast cells. Nat. Chem. Biol. 2, 195-196
32. Anower-E-Khuda M. F., Habuchi, H., Nagai, N., Habuchi, O., Yokochi, T., and Kimata, K. (2013) Heparan sulfate 6-O-sulfotransferase isoform-dependent regulatory effects of heparin on the activities of various proteases in mast cells and the biosynthesis of 6-O-sulfated heparin. J. Biol. Chem. 288, 3705-7317
33. Zhang, L., Beeler, D. L., Lawrence, R., Lech, M., Liu, J., Davis, J. C., Shriver, Z., Sasisekharan, R., and Rosenberg, R. D. (2001) 6-O-Sulfotransferase- 1 represents a critical enzyme in the anticoagulant heparan sulfate biosynthetic pathway. J. Biol. Chem. 276, 42311-42321
34. Shworak, N. W., Kobayashi, T., de Agostini, A., and Smits, N. C. (2010) Anticoagulant heparan sulfate to not clot-or not? Prog. Mol. Biol. Transl. Sci. 93, 153-178
35. Shworak, N. W., HajMohammadi, S., de Agostini, A. I., and Rosenberg, R. D. (2002) Mice deficient in heparan sulfate 3-O-sulfotransferase-1: normal hemostasis with unexpected perinatal phenotypes. Glycoconj. J. 19, 355-361
36. Datta, P., Linhardt, R. J., and Sharfstein, S. T. (2013) An 'omics approach towards CHO cell engineering. Biotechnol. Bioeng. 110, 1255-1271
37. Zhang, L., Lawrence, R., Frazier, B. A., and Esko, J. D. (2006) CHO glycosylation mutants: proteoglycans. Methods Enzymol. 416, 205-221
38. Xu, X., Nagarajan, H., Lewis, N. E., Pan, S., Cai, Z., Liu, X., Chen, W., Xie, M., Wang, W., Hammond, S., Andersen, M. R., Neff, N., Passarelli, B., Koh, W., Fan, H. C., Wang, J., Gui, Y., Lee, K. H., Betenbaugh, M. J., Quake, S. R., Famili, I., Palsson, B. O., and Wang, J. (2011) The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line. Nat. Biotechnol. 29, 735-741
39. Baik, J. Y., Gasimli, L., Yang, B., Datta, P., Zhang, F., Glass, C. A., Esko, J. D., Linhardt, R. J., and Sharfstein, S. T. (2012) Metabolic engineering of Chinese hamster ovary cells: towards a bioengineered heparin. Metab. Eng. 14, 81-90
40. Busse, M., Feta, A., Presto, J., Wilén, M., Grønning, M., Kjellén, L., and Kusche-Gullberg, M. (2007) Contribution of EXT1, EXT2, and EXTL3 to heparan sulfate chain elongation. J. Biol. Chem. 282, 32802-32810
41. Yang, B., Chang, Y., Weyers, A. M., Sterner, E., and Linhardt, R. J. (2012) Disaccharide analysis of glycosaminoglycan mixtures by ultra-high-performance liquid chromatography-mass spectrometry. J. Chromatogr. A 1225, 91-98
42. Zhao, X., Yang, B., Linkens, K., Datta, P., Onishi, A., Zhang, F., and Linhardt, R. J. (2013) Microscale separation of heparosan, heparan sulfate, and heparin. Anal. Biochem. 434, 215-217
43. Zhang, F., Yang, B., Ly, M., Solakyildirim, K., Xiao, Z., Wang, Z., Beaudet, J. M., Torelli, A. Y., Dordick, J. S., and Linhardt, R. J. (2011) Structural characterization of heparins from different commercial sources. Anal. Bioanal. Chem. 401, 2793-2803
44. Fu, L., Li, G., Yang, B., Onishi, A., Li, L., Sun, P., Zhang, F., and Linhardt, R. J. (2013) Structural characterization of pharmaceutical heparins prepared from different animal tissues. J. Pharm. Sci. 102, 1447-1457
45. Datta, P. (2013) Cell Engineering and Modulation of Metabolic Pathways in Mammalian Cells for the Production of Glycoprotein and Proteoglycan Based Pharmaceuticals. Doctoral thesis, Rensselaer Polytechnic Institute
46. Montgomery, R. I., Lidholt, K., Flay, N. W., Liang, J., Vertel, B., Lindahl, U., and Esko, J. D. (1992) Stable heparin-producing cell lines derived from the Furth murine mastocytoma. Proc. Natl. Acad. Sci. U.S.A. 89, 11327-11331
47. Esko, J. D., Weinke, J. L., Taylor, W. H., Ekborg, G., Rodén, L., Anantharamaiah, G., and Gawish, A. (1987) Inhibition of chondroitin and heparan sulfate biosynthesis in Chinese hamster ovary cell mutants defective in galactosyltransferase I. J. Biol. Chem. 262, 12189-12195
48. Esko, J. D., Stewart, T. E., and Taylor, W. H. (1985) Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 82, 3197-3201
49. Cuellar, K., Chuong, H., Hubbell, S. M., and Hinsdale, M. E. (2007) Biosynthesis of chondroitin and heparan sulfate in Chinese hamster ovary cells depends on xylosyltransferase II. J. Biol. Chem. 282, 5195-5200
50. Zhao, W., Garron, M. L., Yang, B., Xiao, Z., Esko, J. D., Cygler, M., and Linhardt, R. J. (2011) Asparagine 405 of heparin lyase II prevents the cleavage of glycosidic linkages proximate to a 3-O-sulfoglucosamine residue. FEBS Lett. 585, 2461-2466
51. Moon, A. F., Xu, Y., Woody, S. M., Krahn, J. M., Linhardt, R. J., Liu, J., and Pedersen, L. C. (2012) Dissecting the substrate recognition of 3-O-sulfotransferase for the biosynthesis of anticoagulant heparin. Proc. Natl. Acad. Sci. U.S.A. 109, 5265-5270
52. Chen, J., and Liu, J. (2005) Characterization of the structure of antithrombin-binding heparan sulfate generated by heparan sulfate 3-O-sulfotransferase 5. Biochim. Biophys. Acta 1725, 190-200
53. Zhang, L., Lawrence, R., Schwartz, J. J., Bai, X., Wei, G., Esko, J. D., and Rosenberg, R. D. (2001) The effect of precursor structures on the action of glucosaminyl 3-O-sulfotransferase-1 and the biosynthesis of anticoagulant heparan sulfate. J. Biol. Chem. 276, 28806-28813
54. Presto, J., Thuveson, M., Carlsson, P., Busse, M., Wilén, M., Eriksson, I., Kusche-Gullberg, M., and Kjellén, L. (2008) Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation. Proc. Natl. Acad. Sci. U.S.A. 105, 4751-4756