Molecular mechanism of substrate specificity for heparan sulfate 2-O-sulfotransferase

Journal of Biological Chemistry

Volumn 289, Issue 19, 2014, Pages 13407-13418

  Liu, Chunhui ^a,b   Sheng, Juzheng ^a,b   Krahn, Juno M ^c   Perera, Lalith ^c   Xu, Yongmei ^a   Hsieh, Po Hung ^a   Dou, Wenfang ^a,d   Liu, Jian ^a   Pedersen, Lars C ^c  

^a University of North Carolina   (United States)

^b SHANDONG UNIVERSITY   (China)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d JIANGNAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; ENZYMES;

BIOSYNTHESIS PATHWAYS; ELECTROSTATIC REPULSION; HEPTASACCHARIDES; MOLECULAR MECHANISM; PHYSIOLOGICAL FUNCTIONS; SITE DIRECTED MUTAGENESIS; STRUCTURAL EVIDENCE; SUBSTRATE SPECIFICITY;

HYDRAULIC STRUCTURES;

HEPARAN SULFATE; HEPARAN SULFATE 2 O SULFOTRANSFERASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME BINDING; ENZYME MODIFICATION; ENZYME SPECIFICITY; ENZYME SYNTHESIS; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

HEPARAN SULFATE; HEPARIN; HEPARIN-BINDING PROTEIN; OLIGOSACCHARIDE; SULFOTRANSFERASE;

ANIMALS; CATALYTIC DOMAIN; CHICKENS; CRYSTALLOGRAPHY, X-RAY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; SULFOTRANSFERASES;

EID: 84900432862     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.530535     Document Type: Article

References (38)

1. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037
2. Liu, J., Moon, A. F., Sheng, J., and Pedersen, L. C. (2012) Understanding the substrate specificity of the heparan sulfate sulfotransferases by a combined synthetic crystallographic approach. Curr. Opin. Struct. Biol. 22, 550-557
3. Esko, J. D., and Lindahl, U. (2001) Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169-173
4. Kreuger, J., Salmivirta, M., Sturiale, L., Giménez-Gallego, G., and Lindahl, U. (2001) Sequence analysis of heparan sulfate epitopes with graded affinities for fibroblast growth factors 1 and 2. J. Biol. Chem. 276, 30744-30752
5. Witt, R. M., Hecht, M. L., Pazyra-Murphy, M. F., Cohen, S. M., Noti, C., Van Kuppevelt, T. H., Fuller, M., Chan, J. A., Hopwood, J. J., Seeberger, P. H., and Segal, R. A. (2013) Heparan sulfate proteoglycans containing a glycpican 5 core and 2-O-sulfoiduronic acid function as sonic hedgehog co-receptors to promote proliferation. J. Biol. Chem. 288, 26275-26288
6. Bullock, S. L., Fletcher, J. M., Beddington, R. S., and Wilson, V. A. (1998) Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev. 12, 1894-1906
7. Axelsson, J., Xu, D., Kang, B. N., Nussbacher, J. K., Handel, T. M., Ley, K., Sriramarao, P., and Esko, J. D. (2012) Inactivation of heparan sulfate 2-Osulfotransferase accentuates neutrophil infiltration during acute inflammation in mice. Blood 120, 1742-1751
8. Bülow, H. E., and Hobert, O. (2004) Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron 41, 723-736
9. Kinnunen, T., Huang, Z., Townsend, J., Gatdula, M. M., Brown, J. R., Esko, J. D., and Turnbull, J. E. (2005) Heparan 2-O-sulfotransferase, hst-2, is essential for normal cell migration in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 102, 1507-1512
10. Kamimura, K., Koyama, T., Habuchi, H., Ueda, R., Masu, M., Kimata, K., and Nakato, H. (2006) Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. J. Cell Biol. 174, 773-778
11. Linhardt, R. J., and Liu, J. (2012) Synthetic heparin. Curr. Opin. Pharmacol. 12, 217-219
12. Liu, H., Zhang, Z., and Linhardt, R. J. (2009) Lessons learned from the contamination of heparin. Nat. Prod. Rep. 26, 313-321
13. Chen, J., Avci, F. Y., Muñoz, E. M., McDowell, L. M., Chen, M., Pedersen, L. C., Zhang, L., Linhardt, R. J., and Liu, J. (2005) Enzymatically redesigning of biologically active heparan sulfate. J. Biol. Chem. 280, 42817-42825
14. Chen, J., Jones, C. L., and Liu, J. (2007) Using an enzymatic combinatorial approach to identify anticoagulant heparan sulfate structures. Chem. Biol. 14, 986-993
15. Zhang, Z., McCallum, S. A., Xie, J., Nieto, L., Corzana, F., Jiménez-Barbero, J., Chen, M., Liu, J., and Linhardt, R. J. (2008) Solution structure of chemoenzymatically synthesized heparin and its precursors. J. Am. Chem. Soc. 130, 12998-13007
16. Xu, Y., Masuko, S., Takieddin, M., Xu, H., Liu, R., Jing, J., Mousa, S. A., Linhardt, R. J., and Liu, J. (2011) Chemoenzymatic synthesis of homogeneous ultra-low molecular weight heparin. Science 334, 498-501
17. Shriver, Z., Raguram, S., and Sasisekharan, R. (2004) Glycomics: a pathway to a class of new and improved therapeutics. Nat. Rev. Drug Discov. 3, 863-873
18. Bethea, H. N., Xu, D., Liu, J., and Pedersen, L. C. (2008) Redirecting the substrate specificity of heparan sulfate 2-O-sulfotransferase by structurally guided mutagenesis. Proc. Natl. Acad. Sci. U. S. A. 105, 18724-18729
19. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
20. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D. Biol Crystallogr 60, 2126-2132
21. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-Atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
22. Shively, J. E., and Conrad, H. E. (1976) Formation of anhydrosugars in the chemical depolymerization of heparin. Biochemistry 15, 3932-3942
23. 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
24. Case, D. A., Darden, T. A., Cheatham, T. E. 3rd, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Hayik, S., Roitberg, A., Seabra, G., Swails, J., Goetz, A. W., Kolossváry, I., Wong, K. F., Paesani, F., Vanicek, J., Wolf, R. M., Liu, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Cai, Q., Ye, X., Wang, J., Hsieh, M.-J., Cui, G., Roe, D. R., Mathews, D. H., Seetin, M. G., Salomon-Ferrer, R., Sagui, C., Babin, V., Luchko, T., Gusarov, S., Kovalenko, A., and Kollman, P. A. (2012) AMBER 12, University of California, San Francisco
25. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G. A., Nakatsuji, H., Caricato, M., Li, X., Hratchian, H. P., Izmaylov, A. F., Bloino, J., Zheng, G., Sonnenberg, J. L., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Vreven, T., Montgomery, J., J. A., Peralta, J. E., Ogliaro, F., Bearpark, M., Heyd, J. J., Brothers, E., Kudin, K. N., Staroverov, V. N., Kobayashi, R., Normand, J., Raghavachari, K., Rendell, A., Burant, J. C., Iyengar, S. S., Tomasi, J., Cossi, M., Rega, N., Millam, J. M., Klene, M., Knox, J. E., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Martin, R. L., Morokuma, K., Zakrzewski, V. G., Voth, G. A., Salvador, P., Dannenberg, J. J., Dapprich, S., Daniels, A. D., Farkas, O., Foresman, J. B., Ortiz, J. V., Cioslowski, J., and Fox, D. J. (2009) Gaussian 09, Revision C, 1, Gaussian, Inc., Wallingford CT
26. Peterson, S., and Liu, J. (2012) Deciphering mode of action heparanase using structurally defined oligosaccharides. J. Biol. Chem. 287, 34836-34843
27. Moon, A. F., Mueller, G. A., Zhong, X., and Pedersen, L. C. (2010) A synergistic approach to protein crystallization: combination of a fixedarm carrier with surface entropy reduction. Protein Sci. 19, 901-913
28. Moon, A. F., Edavettal, S. C., Krahn, J. M., Munoz, E. M., Negishi, M., Linhardt, R. J., Liu, J., and Pedersen, L. C. (2004) Structural analysis of the sulfotransferase (3-OST-3) involved in the biosynthesis of an entry receptor of herpes simplex virus 1. J. Biol. Chem. 279, 45185-45193
29. Moon, A. F., Xu, Y., Woody, S. M., Krahn, J. M., Linhardt, R. J., Liu, J., and Pedersen, L. C. (2012) Dissecting substrate recognition mode of heparan sulfate 3-O-sulfotransferases for the biosynthesis of anticoagulant heparin. Proc. Natl. Acad. Sci. U. S. A. 109, 5265-5270
30. 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
31. Liu, R., Xu, Y., Chen, M., Weïwer, M., Zhou, X., Bridges, A. S., De Angelis, P. L., Zhang, Q., Linhardt, R. J., and Liu, J. (2010) Chemoenzymatic design of heparan sulfate oligosaccharides. J. Biol. Chem. 285, 34240-34249
32. Sheng, J., Xu, Y., Dulaney, S. B., Huang, X., and Liu, J. (2012) Uncovering biphasic catalytic mode of C5-epimerase in heparan sulfate biosynthesis. J. Biol. Chem. 287, 20996-21002
33. Li, J. P., Gong, F., El Darwish, K., Jalkanen, M., and Lindahl, U. (2001) Characterization of the D-glucuronyl C5-epimerase involved in the biosynthesis of heparin and heparan sulfate. J. Biol. Chem. 276, 20069-20077
34. Li, K., Bethea, H. N., and Liu, J. (2010) Determining the activity of C5-epimerase using an engineered heparan sulfate 2-O-sulfotransferase. J. Biol. Chem. 285, 11106-11113
35. Kreuger, J., Spillmann, D., Li, J. P., and Lindahl, U. (2006) Interactions between heparan sulfate and proteins: the concept of specificity J. Cell Biol. 174, 323-327
36. Mulloy, B., and Forster, M. (2000) Conformation and dynamics of heparin and heparan sulfate. Glycobiology 10, 1147-1156
37. Linhardt, R. J. (2003) 2003 Claude S. Hudson Award address in carbohydrate chemistry. Heparin: structure and activity. J. Med. Chem. 46, 2551-2564
38. Lindahl, U., Kusche-Gullberg, M., and Kjellén, L. (1998) Regulated diversity of heparan sulfate. J. Biol. Chem. 273, 24979-24982