Heparan Sulfate Domains Required for Fibroblast Growth Factor 1 and 2 Signaling Through Fibroblast Growth Factor Receptor 1c

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2016 Dec 30

PMID 28031461

Citations 24

Authors

Victor Schultz

Mathew Suflita

Xinyue Liu

Xing Zhang

Yanlei Yu

Lingyun Li

Dixy E Green

Yongmei Xu

Fuming Zhang

Paul L DeAngelis

Jian Liu

Robert J Linhardt

Affiliations

Soon will be listed here.

Abstract

A small library of well defined heparan sulfate (HS) polysaccharides was chemoenzymatically synthesized and used for a detailed structure-activity study of fibroblast growth factor (FGF) 1 and FGF2 signaling through FGF receptor (FGFR) 1c. The HS polysaccharide tested contained both undersulfated (NA) domains and highly sulfated (NS) domains as well as very well defined non-reducing termini. This study examines differences in the HS selectivity of the positive canyons of the FGF1-FGFR1c and FGF2-FGFR1c HS binding sites of the symmetric FGF-FGFR-HS signal transduction complex. The results suggest that FGF1-FGFR1c binding site prefers a longer NS domain at the non-reducing terminus than FGF2-FGFR1c In addition, FGF2-FGFR1c can tolerate an HS chain having an -acetylglucosamine residue at its non-reducing end. These results clearly demonstrate the different specificity of FGF1-FGFR1c and FGF2-FGFR1c for well defined HS structures and suggest that it is now possible to chemoenzymatically synthesize precise HS polysaccharides that can selectively mediate growth factor signaling. These HS polysaccharides might be useful in both understanding and controlling the growth, proliferation, and differentiation of cells in stem cell therapies, wound healing, and the treatment of cancer.

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References

Hileman R, Smith A, Toida T, Linhardt R . Preparation and structure of heparin lyase-derived heparan sulfate oligosaccharides. Glycobiology. 1997; 7(2):231-9. DOI: 10.1093/glycob/7.2.231. View

Yang B, Chang Y, Weyers A, Sterner E, Linhardt R . Disaccharide analysis of glycosaminoglycan mixtures by ultra-high-performance liquid chromatography-mass spectrometry. J Chromatogr A. 2012; 1225:91-8. PMC: 3268819. DOI: 10.1016/j.chroma.2011.12.063. View

Xu Y, Masuko S, Takieddin M, Xu H, Liu R, Jing J . Chemoenzymatic synthesis of homogeneous ultralow molecular weight heparins. Science. 2011; 334(6055):498-501. PMC: 3425363. DOI: 10.1126/science.1207478. View

GRIFFIN C, Linhardt R, Van Gorp C, Toida T, Hileman R, Schubert 2nd R . Isolation and characterization of heparan sulfate from crude porcine intestinal mucosal peptidoglycan heparin. Carbohydr Res. 1995; 276(1):183-97. DOI: 10.1016/0008-6215(95)00166-q. View

Mohammadi M, Olsen S, Ibrahimi O . Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev. 2005; 16(2):107-37. DOI: 10.1016/j.cytogfr.2005.01.008. View

Sterner E, Masuko S, Li G, Li L, Green D, Otto N . Fibroblast growth factor-based signaling through synthetic heparan sulfate blocks copolymers studied using high cell density three-dimensional cell printing. J Biol Chem. 2014; 289(14):9754-65. PMC: 3975022. DOI: 10.1074/jbc.M113.546937. View

Jing W, DeAngelis P . Synchronized chemoenzymatic synthesis of monodisperse hyaluronan polymers. J Biol Chem. 2004; 279(40):42345-9. DOI: 10.1074/jbc.M402744200. View

Esko J, Selleck S . Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem. 2002; 71:435-71. DOI: 10.1146/annurev.biochem.71.110601.135458. View

Shworak N, Liu J, Fritze L, Schwartz J, Zhang L, Logeart D . Molecular cloning and expression of mouse and human cDNAs encoding heparan sulfate D-glucosaminyl 3-O-sulfotransferase. J Biol Chem. 1997; 272(44):28008-19. DOI: 10.1074/jbc.272.44.28008. View

10.

Marie P . Fibroblast growth factor signaling controlling osteoblast differentiation. Gene. 2003; 316:23-32. DOI: 10.1016/s0378-1119(03)00748-0. View

11.

Zhang X, Ibrahimi O, Olsen S, Umemori H, Mohammadi M, Ornitz D . Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem. 2006; 281(23):15694-700. PMC: 2080618. DOI: 10.1074/jbc.M601252200. View

12.

Ornitz D, Itoh N . Fibroblast growth factors. Genome Biol. 2001; 2(3):REVIEWS3005. PMC: 138918. DOI: 10.1186/gb-2001-2-3-reviews3005. View

13.

Staples G, Shi X, Zaia J . Glycomics analysis of mammalian heparan sulfates modified by the human extracellular sulfatase HSulf2. PLoS One. 2011; 6(2):e16689. PMC: 3035651. DOI: 10.1371/journal.pone.0016689. View

14.

Rosenberg R, Armand G, Lam L . Structure-function relationships of heparin species. Proc Natl Acad Sci U S A. 1978; 75(7):3065-9. PMC: 392714. DOI: 10.1073/pnas.75.7.3065. View

15.

Lindahl U, Li J . Interactions between heparan sulfate and proteins-design and functional implications. Int Rev Cell Mol Biol. 2009; 276:105-59. DOI: 10.1016/S1937-6448(09)76003-4. View

16.

Liu R, Xu Y, Chen M, Weiwer M, Zhou X, Bridges A . Chemoenzymatic design of heparan sulfate oligosaccharides. J Biol Chem. 2010; 285(44):34240-9. PMC: 2962522. DOI: 10.1074/jbc.M110.159152. View

17.

Puvirajesinghe T, Ahmed Y, Powell A, Fernig D, Guimond S, Turnbull J . Array-based functional screening of heparin glycans. Chem Biol. 2012; 19(5):553-8. DOI: 10.1016/j.chembiol.2012.03.011. View

18.

Ramani V, Purushothaman A, Stewart M, Thompson C, Vlodavsky I, Au J . The heparanase/syndecan-1 axis in cancer: mechanisms and therapies. FEBS J. 2013; 280(10):2294-306. PMC: 3651779. DOI: 10.1111/febs.12168. View

19.

Naimy H, Buczek-Thomas J, Nugent M, Leymarie N, Zaia J . Highly sulfated nonreducing end-derived heparan sulfate domains bind fibroblast growth factor-2 with high affinity and are enriched in biologically active fractions. J Biol Chem. 2011; 286(22):19311-9. PMC: 3103309. DOI: 10.1074/jbc.M110.204693. View

20.

Liu J, Moon A, Sheng J, Pedersen L . Understanding the substrate specificity of the heparan sulfate sulfotransferases by an integrated biosynthetic and crystallographic approach. Curr Opin Struct Biol. 2012; 22(5):550-7. PMC: 3711681. DOI: 10.1016/j.sbi.2012.07.004. View