Sulfation patterns of glycosaminoglycans encode molecular recognition and activity

Nature Chemical Biology

Volumn 2, Issue 9, 2006, Pages 467-473

  Gama, Cristal I ^a   Tully, Sarah E ^b   Sotogaku, Naoki ^b   Clark, Peter M ^a   Rawat, Manish ^a   Vaidehi, Nagarajan ^c,d   Goddard, William A ^c   Nishi, Akinori ^b   Hsieh Wilson, Linda C ^a  

^a California Institute of Technology   (United States)

^b KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; GROWTH FACTOR; OLIGOSACCHARIDE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NERVE CELL GROWTH; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; RAT; RNA SEQUENCE; SULFATION;

EID: 33747618728     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio810     Document Type: Article

References (33)

1. Hacker, U., Nybakken, K. & Perrimon, N. Heparan sulphate proteoglycans: the sweet side of development. Nat. Rev. Mol. Cell Biol. 6, 530-541 (2005).
2. Capila, I. & Linhardt, R.J. Heparin-protein interactions. Angew. Chem. Int. Edn Engl. 41, 391-412 (2002).
3. Sasisekharan, R., Shriver, Z., Venkataraman, G. & Narayanasami, U. Roles of heparan-sulphate glycosaminoglycans in cancer. Nat. Rev. Cancer 2, 521-528 (2002).
4. Bradbury, E.J. et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640 (2002).
5. Kitagawa, H., Tsutsumi, K., Tone, Y. & Sugahara, K. Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain. J. Biol. Chem. 272, 31377-31381 (1997).
6. Plaas, A.H.K., West, L.A., Wong-Palms, S. & Nelson, F.R.T. Glycosaminoglycan sulfation in human osteoarthritis. Disease-related alterations at the non-reducing termini of chondroitin and dermatan sulfate. J. Biol. Chem. 273, 12642-12649 (1998).
7. Holt, C.E. & Dickson, B.J. Sugar codes for axons? Neuron 46, 169-172 (2005).
8. Nandini, C.D. et al. Structural and functional characterization of oversulfated chondroitin sulfate/dermatan sulfate hybrid chains from the notochord of hagfish. Neuritogenic and binding activities for growth factors and neurotrophic factors. J. Biol. Chem. 279, 50799-50809 (2004).
9. Ueoka, C. et al. Neuronal cell adhesion, mediated by the heparin-binding neuroregulatory factor midkine, is specifically inhibited by chondroitin sulfate E. Structural and functional implications of the over-sulfated chondroitin sulfate. J. Biol. Chem. 275, 37407-37413 (2000).
10. Shuo, T. et al. Developmental changes in the biochemical and immunological characters of the carbohydrate moiety of neuroglycan C, a brain-specific chondroitin sulfate proteoglycan. Glycoconj. J. 20, 267-278 (2004).
11. Tsuchida, K. et al. Appican, the proteoglycan form of the amyloid precursor protein, contains chondroitin sulfate E in the repeating disaccharide region and 4-O-sulfated galactose in the linkage region. J. Biol. Chem. 276, 37155-37160 (2001).
12. Deepa, S.S., Yamada, S., Zako, M., Goldberger, O. & Sugahara, K. Chondroitin sulfate chains on syndecan-1 and syndecan-4 from normal murine mammary gland epithelial cells are structurally and functionally distinct and cooperate with heparan sulfate chains to bind growth factors. A novel function to control binding of midkine, pleiotrophin, and basic fibroblast growth factor. J. Biol. Chem. 279, 37368-37376 (2004).
13. Karst, N.A. & Linhardt, R.J. Recent chemical and enzymatic approaches to the synthesis of glycosaminoglycan oligosaccharides. Curr. Med. Chem. 10, 1993-2031 (2003).
14. Tully, S.E. et al. A chondroitin sulfate small molecule that stimulates neuronal growth. J. Am. Chem. Soc. 126, 7736-7737 (2004).
15. Jacquinet, J.-C., Rochepeau-Jobron, L. & Combal, J.-P. Multigram syntheses of the disaccharide repeating units of chondroitin 4- and 6-sulfates. Carbohydr. Res. 314, 283-288 (1998).
16. Brickman, Y.G. et al. Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J. Biol. Chem. 273, 4350-4359 (1998).
17. Kantor, D.B. et al. Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44, 961-975 (2004).
18. Mayo, S.L., Olafson, B.D. & Goddard, W.A., III DREIDING: A generic force field for molecular simulations. J. Phys. Chem. 94, 8897-8909 (1990).
19. Rappe, A.K. & Goddard, W.A., III Charge equilibration for molecular dynamics simulations. J. Phys. Chem. 95, 3358-3363 (1991).
20. Lim, K.-T. et al. Molecular dynamics for very large systems on massively parallel computers: the MPSim program. J. Comput. Chem. 18, 501-521 (1997).
21. Feizi, T., Fazio, F., Chai, W. & Wong, C.H. Carbohydrate microarrays - a new set of technologies at the frontiers of glycomics. Curr. Opin. Struct. Biol. 13, 637-645 (2003).
22. de Paz, J.L., Noti, C. & Seeberger, P.H. Microarrays of synthetic heparin oligosaccharides. J. Am. Chem. Soc. 128, 2766-2767 (2006).
23. Park, S., Lee, M.R., Pyo, S.J. & Shin, I. Carbohydrate chips for studying high-throughput carbohydrate-protein interactions. J. Am. Chem. Soc. 126, 4812-4819 (2004).
24. Muramatsu, T. Midkine and pleiotrophin: two related proteins involved in development, survival, inflammation and tumorigenesis. J. Biochem. 132, 359-371 (2002).
25. Herndon, M.E., Stipp, C.S. & Lander, A.D. Interactions of neural glycosaminoglycans and proteoglycans with protein ligands: assessment of selectivity, heterogeneity and the participation of core proteins in binding. Glycobiology 9, 143-155 (1999).
26. Huang, E.J. & Reichardt, L.F. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736 (2001).
27. Bicknese, A.R., Sheppard, A.M., O'Leary, D.D. & Pearlman, A.L. Thalamocortical axons extend along a chondroitin sulfate proteoglycan-enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J. Neurosci. 14, 3500-3510 (1994).
28. Jiang, B., Akaneya, Y., Hata, Y. & Tsumoto, T. Long-term depression is not induced by low-frequency stimulation in rat visual cortex in vivo: a possible preventing role of endogenous brain-derived neurotrophic factor. J. Neurosci. 23, 3761-3770 (2003).
29. Seil, F.J. & Drake-Baumann, R. TrkB receptor ligands promote activity-dependent inhibitory synaptogenesis. J. Neurosci. 20, 5367-5373 (2000).
30. Skoff, A.M. & Adler, J.E. Nerve growth factor regulates substance P in adult sensory neurons through both TrkA and p75 receptors. Exp. Neurol. 197, 430-436 (2006).
31. Bellaiche, Y., The, I. & Perrimon, N. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature 394, 85-88 (1998).
32. Fernaud-Espinosa, I., Nieto-Sampedro, M. & Bovolenta, P. Developmental distribution of glycosaminoglycans in embryonic rat brain: relationship to axonal tract formation. J. Neurobiol. 30, 410-424 (1996).
33. Greeley, B.H. et al. New pseudospectral algorithms for electronic structure calculations: length scale separation and analytical two-electron integral corrections. J. Chem. Phys. 101, 4028-4041 (1994).