Specific sides to multifaceted glycosaminoglycans are observed in embryonic development

Seminars in Cell and Developmental Biology

Volumn 21, Issue 6, 2010, Pages 631-637

  Kramer, Kenneth L ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Chondroitin sulfate; Glycosaminoglycan; Heparan sulfate; Hyaluronan; Keratan sulfate

Indexed keywords

GLYCOSAMINOGLYCAN; POLYSACCHARIDE;

CARDIOVASCULAR SYSTEM; CELL DIFFERENTIATION; CELL MIGRATION; CELL STRUCTURE; EMBRYO DEVELOPMENT; EPIMERIZATION; HOMEOSTASIS; NERVE FIBER; NONHUMAN; ORGANOGENESIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; STEM CELL; SULFATION;

EID: 77955281892     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2010.06.002     Document Type: Review

References (121)

1. Sasisekharan R., Raman R., Prabhakar V. Glycomics approach to structure-function relationships of glycosaminoglycans. Annu Rev Biomed Eng 2006, 8:181-231.
2. Yan D., Lin X. Shaping morphogen gradients by proteoglycans. Cold Spring Harb Perspect Biol 2009, 1:a002493.
3. Sirko S., Holst Av, Weber A., Wizenmann A., Theocharidis U., Götz M., et al. Chondroitin sulfates are required for fibroblast growth factor-2-dependent proliferation and maintenance in neural stem cells and for epidermal growth factor-dependent migration of their progeny. Stem Cells 2010, 28:775-787.
4. Gualeni B, Facchini M, De Leonardis F, Tenni R, Cetta G, Viola M, et al. Defective proteoglycan sulfation of the growth plate zones causes reduced chondrocyte proliferation via an altered Indian hedgehog signalling. Matrix Biol; in press.
5. Hayashida Y., Akama T.O., Beecher N., Lewis P., Young R.D., Meek K.M., et al. Matrix morphogenesis in cornea is mediated by the modification of keratan sulfate by GlcNAc 6-O-sulfotransferase. Proc Natl Acad Sci USA 2006, 103:13333-13338.
6. Maccarana M., Kalamajski S., Kongsgaard M., Magnusson S.P., Oldberg A., Malmstrom A. Dermatan sulfate epimerase 1-deficient mice have reduced content and changed distribution of iduronic acids in dermatan sulfate and an altered collagen structure in skin. Mol Cell Biol 2009, 29:5517-5528.
7. Osterholm C., Barczyk M.M., Busse M., Gronning M., Reed R.K., Kusche-Gullberg M. Mutation in the heparan sulfate biosynthesis enzyme EXT1 influences growth factor signaling and fibroblast interactions with the extracellular matrix. J Biol Chem 2009, 284:34935-34943.
8. Bulow H.E., Hobert O. The molecular diversity of glycosaminoglycans shapes animal development. Annu Rev Cell Dev Biol 2006, 22:375-407.
9. Petitou M., Nancy-Portebois V., Dubreucq G., Motte V., Meuleman D., De Kort M., et al. From heparin to EP217609: the long way to a new pentasaccharide-based neutralisable anticoagulant with an unprecedented pharmacological profile. Thromb Haemost 2009, 102:804-810.
10. Richard B., Swanson R., Olson S.T. The signature 3-O-sulfo group of the anticoagulant heparin sequence is critical for heparin binding to antithrombin but is not required for allosteric activation. J Biol Chem 2009, 284:27054-27064.
11. Guerrini M., Beccati D., Shriver Z., Naggi A., Viswanathan K., Bisio A., et al. Oversulfated chondroitin sulfate is a contaminant in heparin associated with adverse clinical events. Nat Biotechnol 2008, 26:669-675.
12. Li B., Suwan J., Martin J.G., Zhang F., Zhang Z., Hoppensteadt D., et al. Oversulfated chondroitin sulfate interaction with heparin-binding proteins: new insights into adverse reactions from contaminated heparins. Biochem Pharmacol 2009, 78:292-300.
13. Ashikari-Hada S., Habuchi H., Sugaya N., Kobayashi T., Kimata K. Specific inhibition of FGF-2 signaling with 2-O-sulfated octasaccharides of heparan sulfate. Glycobiology 2009, 19:644-654.
14. Noden D.M. Viktor Hamburger (1900-2001). Trends Neurosci 2001, 24:673-674.
15. Ledin J., Staatz W., Li J.-P., Gotte M., Selleck S., Kjellen L., et al. Heparan sulfate structure in mice with genetically modified heparan sulfate production. J Biol Chem 2004, 279:42732-42741.
16. Lawrence R., Olson S.K., Steele R.E., Wang L., Warrior R., Cummings R.D., et al. Evolutionary differences in glycosaminoglycan fine structure detected by quantitative glycan reductive isotope labeling. J Biol Chem 2008, 283:33674-33684.
17. Shi X., Zaia J. Organ-specific heparan sulfate structural phenotypes. J Biol Chem 2009, 284:11806-11814.
18. Yamada S., Onishi M., Fujinawa R., Tadokoro Y., Okabayashi K., Asashima M., et al. Structural and functional changes of sulfated glycosaminoglycans in Xenopus laevis during embryogenesis. Glycobiology 2009, 19:488-498.
19. Gandhi N.S., Mancera R.L. The structure of glycosaminoglycans and their interactions with proteins. Chem Biol Drug Des 2008, 72:455-482.
20. Gallagher J.T. Multiprotein signalling complexes: regional assembly on heparan sulphate. Biochem Soc Trans 2006, 34:438-441.
21. Fosang A.J., Last K., Poon C.J., Plaas A.H. Keratan sulphate in the interglobular domain has a microstructure that is distinct from keratan sulphate elsewhere on pig Aggrecan. Matrix Biol 2009, 28:53-61.
22. Pacheco B., Maccarana M., Malmstrom A. Dermatan 4-O-sulfotransferase 1 is pivotal in the formation of iduronic acid blocks in dermatan sulfate. Glycobiology 2009, 19:1197-1203.
23. Carlsson P., Presto J., Spillmann D., Lindahl U., Kjellen L. Heparin/heparan sulfate biosynthesis. J Biol Chem 2008, 283:20008-20014.
24. Woloszynek J.C., Kovacs A., Ohlemiller K.K., Roberts M., Sands M.S. Metabolic adaptations to interrupted glycosaminoglycan recycling. J Biol Chem 2009, 284:29684-29691.
25. Sainio A, Jokela T, Tammi MI, Jarvelainen H. Hyperglycemic conditions modulate connective tissue reorganization by human vascular smooth muscle cells through stimulation of hyaluronan synthesis. Glycobiology; in press.
26. Bishop J.R., Foley E., Lawrence R., Esko J.D. Insulin-dependent diabetes mellitus in mice does not alter liver heparan sulfate. J Biol Chem 2010, 285:14658-14662.
27. Bornemann D.J., Park S., Phin S., Warrior R. A translational block to HSPG synthesis permits BMP signaling in the early Drosophila embryo. Development 2008, 135:1039-1047.
28. Grobe K., Esko J.D. Regulated translation of heparan sulfate N-acetylglucosamine N-deacetylase/n-sulfotransferase isozymes by structured 5'-untranslated regions and internal ribosome entry sites. J Biol Chem 2002, 277:30699-30706.
29. Olson S.K., Bishop J.R., Yates J.R., Oegema K., Esko J.D. Identification of novel chondroitin proteoglycans in Caenorhabditis elegans: embryonic cell division depends on CPG-1 and CPG-2. J Cell Biol 2006, 173:985-994.
30. Esko J.D., Selleck S.B. Order out of chaos: assembly of ligand binding sites in heparan sulfate1. Annu Rev Biochem 2002, 71:435-471.
31. Pinhal M.A., Smith B., Olson S., Aikawa J., Kimata K., Esko J.D. Enzyme interactions in heparan sulfate biosynthesis: uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo. Proc Natl Acad Sci USA 2001, 98:12984-12989.
32. Presto J., Thuveson M., Carlsson P., Busse M., Wilen M., Eriksson I., et al. Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation. Proc Natl Acad Sci USA 2008, 105:4751-4756.
33. Victor X.V., Nguyen T.K., Ethirajan M., Tran V.M., Nguyen K.V., Kuberan B. Investigating the elusive mechanism of glycosaminoglycan biosynthesis. J Biol Chem 2009, 284:25842-25853.
34. Lindahl U., Li J., Kwang W.J. Interactions between heparan sulfate and proteins-design and functional implications. International review of cell and molecular biology 2009, Academic Press, p. 105-159.
35. Prabhakar V., Sasisekharan R. The biosynthesis and catabolism of galactosaminoglycans. Adv Pharmacol 2006, 53:69-115.
36. Kamimura K., Rhodes J.M., Ueda R., McNeely M., Shukla D., Kimata K., et al. Regulation of Notch signaling by Drosophila heparan sulfate 3-O sulfotransferase. J Cell Biol 2004, 166:1069-1079.
37. O'Donnell C.D., Kovacs M., Akhtar J., Valyi-Nagy T., Shukla D. Expanding the role of 3-O sulfated heparan sulfate in herpes simplex virus type-1 entry. Virology 2010, 397:389-398.
38. Maimone M.M., Tollefsen D.M. Structure of a dermatan sulfate hexasaccharide that binds to heparin cofactor II with high affinity. J Biol Chem 1990, 265:18263-18271.
39. Halldorsdottir A.M., Zhang L., Tollefsen D.M. N-Acetylgalactosamine 4,6-O-sulfate residues mediate binding and activation of heparin cofactor II by porcine mucosal dermatan sulfate. Glycobiology 2006, 16:693-701.
40. He L., Giri T.K., Vicente C.P., Tollefsen D.M. Vascular dermatan sulfate regulates the antithrombotic activity of heparin cofactor II. Blood 2008, 111:4118-4125.
41. Asada M., Shinomiya M., Suzuki M., Honda E., Sugimoto R., Ikekita M., et al. Glycosaminoglycan affinity of the complete fibroblast growth factor family. Biochim Biophys Acta (BBA) - Gen Subjects 2009, 1790:40-48.
42. Deakin J.A., Blaum B.S., Gallagher J.T., Uhrin D., Lyon M. The binding properties of minimal oligosaccharides reveal a common heparan sulfate/dermatan sulfate-binding site in hepatocyte growth factor/scatter factor that can accommodate a wide variety of sulfation patterns. J Biol Chem 2009, 284:6311-6321.
43. Conrad AH, Zhang Y, Tasheva ES, Conrad GW. Proteomic analysis of potential keratan sulfate, chondroitin sulfate a, and hyaluronic acid molecular interactions. Invest Ophthalmol Vis Sci; in press.
44. Zinzen R.P., Girardot C., Gagneur J., Braun M., Furlong E.E.M. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 2009, 462:65-70.
45. Badis G., Berger M.F., Philippakis A.A., Talukder S., Gehrke A.R., Jaeger S.A., et al. Diversity and complexity in DNA recognition by transcription factors. Science 2009, 324:1720-1723.
46. Bradley R.K., Li X.-Y., Trapnell C., Davidson S., Pachter L., Chu H.C., et al. Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol 2010, 8:e1000343.
47. Ibrahimi O.A., Yeh B.K., Eliseenkova A.V., Zhang F., Olsen S.K., Igarashi M., et al. Analysis of mutations in fibroblast growth factor (FGF) and a pathogenic mutation in FGF receptor (FGFR) provides direct evidence for the symmetric two-end model for FGFR dimerization. Mol Cell Biol 2005, 25:671-684.
48. Staples G.O., Shi X., Zaia J. Extended NS domains reside at the non-reducing end of heparan sulfate chains. J Biol Chem 2010, 285:18336-18343.
49. Zhang F., Zhang Z., Lin X., Beenken A., Eliseenkova A.V., Mohammadi M., et al. Compositional analysis of heparin/heparan sulfate interacting with fibroblast growth factor. Fibroblast growth factor receptor complexes. Biochemistry 2009, 48:8379-8386.
50. Yan D., Wu Y., Feng Y., Lin S.-C., Lin X. The core protein of glypican dally-like determines its biphasic activity in wingless morphogen signaling. Dev Cell 2009, 17:470-481.
51. Mitsi M., Forsten-Williams K., Gopalakrishnan M., Nugent M.A. A catalytic role of heparin within the extracellular matrix. J Biol Chem 2008, 283:34796-34807.
52. Arrington C.B., Yost H.J. Extra-embryonic syndecan 2 regulates organ primordia migration and fibrillogenesis throughout the zebrafish embryo. Development 2009, 136:3143-3152.
53. Chuang C.Y., Lord M.S., Melrose J., Rees M.D., Knox S.M., Freeman C., et al. Heparan sulfate dependent signaling of fibroblast growth factor (FGF) 18 by chondrocyte-derived Perlecan. Biochemistry 2010, 49:5524-5532.
54. Kolset S., Tveit H. Serglycin-Structure and biology. Cell Mol Life Sci 2008, 65:1073-1085.
55. Kramer K.L., Yost H.J. Heparan sulfate core proteins in cell-cell signaling. Annu Rev Genet 2003, 37:461-484.
56. Roch C., Kuhn J., Kleesiek K., Götting C. Differences in gene expression of human xylosyltransferases and determination of acceptor specificities for various proteoglycans. Biochem Biophys Res Commun 2010, 391:685-691.
57. Gopal S., Bober A., Whiteford J.R., Multhaupt H.A., Yoneda A., Couchman J.R. Heparan sulfate chain valency controls syndecan-4 function in cell adhesion. J Biol Chem 2010, 285:14247-14258.
58. Yan D., Wu Y., Feng Y., Lin S.C., Lin X. The core protein of glypican dally-like determines its biphasic activity in wingless morphogen signaling. Dev Cell 2009, 17:470-481.
59. Williams E.H., Pappano W.N., Saunders A.M., Kim M.S., Leahy D.J., Beachy P.A. Dally-like core protein and its mammalian homologues mediate stimulatory and inhibitory effects on Hedgehog signal response. Proc Natl Acad Sci USA 2010, 107:5869-5874.
60. Gallet A., Staccini-Lavenant L., Thérond P.P. Cellular trafficking of the glypican dally-like is required for full-strength hedgehog signaling and wingless transcytosis. Dev Cell 2008, 14:712-725.
61. Ayers K.L., Gallet A., Staccini-Lavenant L., Thérond P.P. The long-range activity of hedgehog is regulated in the apical extracellular space by the glypican dally and the hydrolase notum. Dev Cell 2010, 18:605-620.
62. Gutierrez J., Brandan E. A novel mechanism of sequestering fibroblast growth factor 2 by glypican in lipid rafts, allowing skeletal muscle differentiation. Mol Cell Biol 2010, 30:1634-1649.
63. Mizuguchi S., Uyama T., Kitagawa H., Nomura K.H., Dejima K., Gengyo-Ando K., et al. Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature 2003, 423:443-448.
64. Izumikawa T., Kanagawa N., Watamoto Y., Okada M., Saeki M., Sakano M., et al. Impairment of embryonic cell division and glycosaminoglycan biosynthesis in glucuronyltransferase-I-deficient mice. J Biol Chem 2010, 285:12190-12196.
65. Morio H., Honda Y., Toyoda H., Nakajima M., Kurosawa H., Shirasawa T. EXT gene family member rib-2 is essential for embryonic development and heparan sulfate biosynthesis in Caenorhabditis elegans. Biochem Biophys Res Commun 2003, 301:317-323.
66. Stickens D., Zak B.M., Rougier N., Esko J.D., Werb Z. Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development 2005, 132:5055-5068.
67. Camenisch T.D., Spicer A.P., Brehm-Gibson T., Biesterfeldt J., Augustine M.L., Calabro A., et al. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest 2000, 106:349-360.
68. Yayon A., Klagsbrun M., Esko J.D., Leder P., Ornitz D.M. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 1991, 64:841-848.
69. Rapraeger A.C., Krufka A., Olwin B.B. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 1991, 252:1705-1708.
70. Norton W.H.J., Ledin J., Grandel H., Neumann C.J. HSPG synthesis by zebrafish Ext2 and Extl3 is required for Fgf10 signalling during limb development. Development 2005, 132:4963-4973.
71. Lin X., Buff E.M., Perrimon N., Michelson A.M. Heparan sulfate proteoglycans are essential for FGF receptor signaling during Drosophila embryonic development. Development 1999, 126:3715-3723.
72. Yan D., Lin X. Drosophila glypican dally-like acts in FGF-receiving cells to modulate FGF signaling during tracheal morphogenesis. Dev Biol 2007, 312:203-216.
73. Kamimura K., Koyama T., Habuchi H., Ueda R., Masu M., Kimata K., et al. Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. J Cell Biol 2006, 174:773-778.
74. Min H., Danilenko D.M., Scully S.A., Bolon B., Ring B.D., Tarpley J.E., et al. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 1998, 12:3156-3161.
75. Patel V.N., Likar K.M., Zisman-Rozen S., Cowherd S.N., Lassiter K.S., Sher I., et al. Specific heparan sulfate structures modulate FGF10-mediated submandibular gland epithelial morphogenesis and differentiation. J Biol Chem 2008, 283:9308-9317.
76. Shah M.M., Sakurai H., Sweeney D.E., Gallegos T.F., Bush K.T., Esko J.D., et al. Hs2st mediated kidney mesenchyme induction regulates early ureteric bud branching. Dev Biol 2010, 339:354-365.
77. Crawford B.E., Garner O.B., Bishop J.R., Zhang D.Y., Bush K.T., Nigam S.K., et al. Loss of the heparan sulfate sulfotransferase, ndst1, in mammary epithelial cells selectively blocks lobuloalveolar development in mice. PLoS One 2010, 5:e10691.
78. Makarenkova H.P., Hoffman M.P., Beenken A., Eliseenkova A.V., Meech R., Tsau C., et al. Differential interactions of FGFs with heparan sulfate control gradient formation and branching morphogenesis. Sci Signal 2009, 2:ra55.
79. Chan J.A., Balasubramanian S., Witt R.M., Nazemi K.J., Choi Y., Pazyra-Murphy M.F., et al. Proteoglycan interactions with Sonic Hedgehog specify mitogenic responses. Nat Neurosci 2009, 12:409-417.
80. Hayashi Y., Kobayashi S., Nakato H. Drosophila glypicans regulate the germline stem cell niche. J Cell Biol 2009, 187:473-480.
81. Guo Z., Wang Z. The glypican dally is required in the niche for the maintenance of germline stem cells and short-range BMP signaling in the Drosophila ovary. Development 2009, 136:3627-3635.
82. Kraushaar D.C., Yamaguchi Y., Wang L. Heparan sulfate is required for embryonic stem cells to exit from self-renewal. J Biol Chem 2010, 285:5907-5916.
83. Lanner F., Lee K.L., Sohl M., Holmborn K., Yang H., Wilbertz J., et al. Heparan sulfation-dependent fibroblast growth factor signaling maintains embryonic stem cells primed for differentiation in a heterogeneous state. Stem Cells 2010, 28:191-200.
84. Baldwin R.J., Dam GBt, Kuppevelt THv, Lacaud G., Gallagher J.T., Kouskoff V., et al. A developmentally regulated heparan sulfate epitope defines a subpopulation with increased blood potential during mesodermal differentiation. Stem Cells 2008, 26:3108-3118.
85. von Holst A., Sirko S., Faissner A. The Unique 473HD-chondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J Neurosci 2006, 26:4082-4094.
86. Gama C.I., Tully S.E., Sotogaku N., Clark P.M., Rawat M., Vaidehi N., et al. Sulfation patterns of glycosaminoglycans encode molecular recognition and activity. Nat Chem Biol 2006, 2:467-473.
87. Ishii M., Maeda N. Oversulfated chondroitin sulfate plays critical roles in the neuronal migration in the cerebral cortex. J Biol Chem 2008, 283:32610-32620.
88. Mizumoto S., Mikami T., Yasunaga D., Kobayashi N., Yamauchi H., Miyake A., et al. Chondroitin 4-O-sulfotransferase-1 is required for somitic muscle development and motor axon guidance in zebrafish. Biochem J 2009, 419:387-399.
89. Fawcett J.W., Asher R.A. The glial scar and central nervous system repair. Brain Res Bull 1999, 49:377-391.
90. Bradbury E.J., Moon L.D.F., Popat R.J., King V.R., Bennett G.S., Patel P.N., et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416:636-640.
91. Sato Y., Oohira A. Chondroitin Sulfate, a major niche substance of neural stem cells, and cell transplantation therapy of neurodegeneration combined with niche modification. Curr Stem Cell Res Ther 2009, 4:200-209.
92. Ito Z., Sakamoto K., Imagama S., Matsuyama Y., Zhang H., Hirano K., et al. N-acetylglucosamine 6-o-sulfotransferase-1-deficient mice show better functional recovery after spinal cord injury. J Neurosci 2010, 30:5937-5947.
93. Lee J.-S., von der Hardt S., Rusch M.A., Stringer S.E., Stickney H.L., Talbot W.S., et al. Axon sorting in the optic tract requires HSPG synthesis by ext2 (dackel) and extl3 (boxer). Neuron 2004, 44:947-960.
94. Kastenhuber E., Kern U., Bonkowsky J.L., Chien C.B., Driever W., Schweitzer J. Netrin-DCC, Robo-Slit, and heparan sulfate proteoglycans coordinate lateral positioning of longitudinal dopaminergic diencephalospinal axons. J Neurosci 2009, 29:8914-8926.
95. Inatani M., Irie F., Plump A.S., Tessier-Lavigne M., Yamaguchi Y. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science 2003, 302:1044-1046.
96. Kalus I., Salmen B., Viebahn C., Figura K.v., Schmitz D., D'Hooge R., et al. Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity. J Cell Mol Med 2009, 13:4505-4521.
97. Pratt T., Conway C.D., Tian N.M.M.-L., Price D.J., Mason J.O. Heparan sulphation patterns generated by specific heparan sulfotransferase enzymes direct distinct aspects of retinal axon guidance at the optic chiasm. J Neurosci 2006, 26:6911-6923.
98. Chanana B., Steigemann P., Jackle H., Vorbraggen G. Reception of slit requires only the chondroitin-sulphate-modified extracellular domain of syndecan at the target cell surface. Proc Natl Acad Sci USA 2009, 106:11984-11988.
99. Bülow H.E., Tjoe N., Townley R.A., Didiano D., van Kuppevelt T.H., Hobert O. Extracellular sugar modifications provide instructive and cell-specific information for axon-guidance choices. Curr Biol 2008, 18:1978-1985.
100. Walsh E.C., Stainier D.Y.R. UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 2001, 293:1670-1673.
101. Camenisch T.D., Schroeder J.A., Bradley J., Klewer S.E., McDonald J.A. Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nat Med 2002, 8:850-855.
102. Iwamoto R., Mine N., Kawaguchi T., Minami S., Saeki K., Mekada E. HB-EGF function in cardiac valve development requires interaction with heparan sulfate proteoglycans. Development 2010, 137:2205-2214.
103. Peal D.S., Burns C.G., Macrae C.A., Milan D. Chondroitin sulfate expression is required for cardiac atrioventricular canal formation. Dev Dyn 2009, 238:3103-3110.
104. Dündar M., Müller T., Zhang Q., Pan J., Steinmann B., Vodopiutz J., et al. Loss of dermatan-4-sulfotransferase 1 function results in adducted thumb-clubfoot syndrome. Am J Hum Genet 2009, 85:873-882.
105. Tuysuz B., Mizumoto S., Sugahara K., Çelebi A., Mundlos S., Turkmen S. Omani-type spondyloepiphyseal dysplasia with cardiac involvement caused by a missense mutation in CHST3. Clin Genet 2009, 75:375-383.
106. Yue X., Schultheiss T.M., McKenzie E.A., Rosenberg R.D. Role of heparan sulfate in dextral heart looping in chick. Glycobiology 2004, 14:745-755.
107. Schuksz M., Fuster M.M., Brown J.R., Crawford B.E., Ditto D.P., Lawrence R., et al. Surfen, a small molecule antagonist of heparan sulfate. Proc Natl Acad Sci USA 2008, 105:13075-13080.
108. Lee T.Y., Folkman J., Javaherian K. HSPG-binding peptide corresponding to the exon 6a-encoded domain of VEGF inhibits tumor growth by blocking angiogenesis in murine model. PLoS One 2010, 5:e9945.
109. Robinson C.J., Mulloy B., Gallagher J.T., Stringer S.E. VEGF165-binding sites within heparan sulfate encompass two highly sulfated domains and can be liberated by k5 lyase. J Biol Chem 2006, 281:1731-1740.
110. Chen E., Stringer S.E., Rusch M.A., Selleck S.B., Ekker S.C. A unique role for 6-O sulfation modification in zebrafish vascular development. Dev Biol 2005, 284:364-376.
111. Habuchi H., Nagai N., Sugaya N., Atsumi F., Stevens R.L., Kimata K. Mice deficient in heparan sulfate 6-o-sulfotransferase-1 exhibit defective heparan sulfate biosynthesis, abnormal placentation, and late embryonic lethality. J Biol Chem 2007, 282:15578-15588.
112. Harfouche R., Hentschel D.M., Piecewicz S., Basu S., Print C., Eavarone D., et al. Glycome and transcriptome regulation of vasculogenesis. Circulation 2009, 120:1883-1892.
113. Jakobsson L., Kreuger J., Holmborn K., Lundin L., Eriksson I., Kjellén L., et al. Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev Cell 2006, 10:625-634.
114. Fan G., Xiao L., Cheng L., Wang X., Sun B., Hu G. Targeted disruption of NDST-1 gene leads to pulmonary hypoplasia and neonatal respiratory distress in mice. FEBS Lett 2000, 467:7-11.
115. Uchimura K., Morimoto-Tomita M., Bistrup A., Li J., Lyon M., Gallagher J., et al. HSulf-2, an extracellular endoglucosamine-6-sulfatase, selectively mobilizes heparin-bound growth factors and chemokines: effects on VEGF, FGF-1, and SDF-1. BMC Biochem 2006, 7:2.
116. Xu D., Moon A.F., Song D., Pedersen L.C., Liu J. Engineering sulfotransferases to modify heparan sulfate. Nat Chem Biol 2008, 4:200-202.
117. Bethea H.N., Xu D., Liu J., Pedersen L.C. Redirecting the substrate specificity of heparan sulfate 2-O-sulfotransferase by structurally guided mutagenesis. Proc Natl Acad Sci USA 2008, 105:18724-18729.
118. Arungundram S., Al-Mafraji K., Asong J., Leach F.E., Amster I.J., Venot A., et al. Modular synthesis of heparan sulfate oligosaccharides for structure-activity relationship studies. J Am Chem Soc 2009, 131:17394-17405.
119. Powell A.K., Ahmed Y.A., Yates E.A., Turnbull J.E. Generating heparan sulfate saccharide libraries for glycomics applications. Nat Protoc 2010, 5:821-833.
120. Thompson S.M., Fernig D.G., Jesudason E.C., Losty P.D., van de Westerlo E.M., van Kuppevelt T.H., et al. Heparan sulfate phage display antibodies identify distinct epitopes with complex binding characteristics: insights into protein binding specificities. J Biol Chem 2009, 284:35621-35631.
121. Petitou M., Casu B., Lindahl U. 1976-1983, a critical period in the history of heparin: the discovery of the antithrombin binding site. Biochimie 2003, 85:83-89.