Dimerized glycosaminoglycan chains increase FGF signaling during zebrafish development

ACS Chemical Biology

Volumn 8, Issue 5, 2013, Pages 939-948

  Nguyen, Thao K N ^a   Tran, Vy M ^a   Sorna, Venkataswamy ^b   Eriksson, Inger ^c   Kojima, Akinori ^d   Koketsu, Mamoru ^d   Loganathan, Duraikkannu ^b   Kjellén, Lena ^c   Dorsky, Richard I ^a   Chien, Chi Bin ^a,e   Kuberan, Balagurunathan ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

^c UPPSALA UNIVERSITY   (Sweden)

^d GIFU UNIVERSITY   (Japan)

^e UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; GLYCOSAMINOGLYCAN; SCAFFOLD PROTEIN; 3 [4 METHYL 2 (2 OXO 3 INDOLINYLMETHYLIDENYL) 3 PYRROLYL]PROPIONIC ACID; FGF8 PROTEIN, ZEBRAFISH; FIBROBLAST GROWTH FACTOR RECEPTOR; GLYCOSIDE; PROTEIN KINASE INHIBITOR; PYRROLE DERIVATIVE; SYNDECAN 1; XYLOSIDES; ZEBRAFISH PROTEIN;

ARTICLE; CONTROLLED STUDY; DEVELOPMENT; DIMERIZATION; EMBRYO; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; WNT SIGNALING PATHWAY; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; DIMERIZATION; EMBRYO, NONMAMMALIAN; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOSAMINOGLYCANS; GLYCOSIDES; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; PROTEIN KINASE INHIBITORS; PYRROLES; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; SYNDECAN-1; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84878072322     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400132r     Document Type: Article

References (49)

1. Perrimon, N. and Bernfield, M. (2000) Specificities of heparan sulphate proteoglycans in developmental processes Nature 404, 725-728 (Pubitemid 30212391)
2. Carey, D. J. (1997) Syndecans: multifunctional cell-surface co-receptors Biochem. J. 327 (Pt 1) 1-16 (Pubitemid 27455453)
3. De Cat, B. and David, G. (2001) Developmental roles of the glypicans Semin. Cell Dev. Biol. 12, 117-125
4. Lee, J. S. and Chien, C. B. (2004) When sugars guide axons: insights from heparan sulphate proteoglycan mutants Nat. Rev. Genet. 5, 923-935
5. Muir, H. (1958) The nature of the link between protein and carbohydrate of a chondroitin sulphate complex from hyaline cartilage Biochem. J. 69, 195-204
6. Lindahl, U., Cifonelli, J. A., Lindahl, B., and Roden, L. (1965) The role of serine in the linkage of heparin to protein J. Biol. Chem. 240, 2817-2820
7. Raman, K. and Kuberan, B. (2010) Chemical tumor biology of heparan sulfate proteoglycans Curr. Chem. Biol. 4, 20-31
8. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology Nature 446, 1030-1037 (Pubitemid 46676065)
9. Sasisekharan, R. and Venkataraman, G. (2000) Heparin and heparan sulfate: biosynthesis, structure and function Curr. Opin. Chem. Biol. 4, 626-631
10. Sanderson, R. D. and Bernfield, M. (1988) Molecular polymorphism of a cell surface proteoglycan: distinct structures on simple and stratified epithelia Proc. Natl. Acad. Sci. U.S.A. 85, 9562-9566 (Pubitemid 19027167)
11. Langford, J. K., Stanley, M. J., Cao, D., and Sanderson, R. D. (1998) Multiple heparan sulfate chains are required for optimal syndecan-1 function J. Biol. Chem. 273, 29965-29971 (Pubitemid 28510014)
12. Gopal, S., Bober, A., Whiteford, J. R., Multhaupt, H. A., Yoneda, A., and Couchman, J. R. (2010) Heparan sulfate chain valency controls syndecan-4 function in cell adhesion J. Biol. Chem. 285, 14247-14258
13. Yayon, A., Klagsbrun, M., Esko, J. D., Leder, P., and Ornitz, D. M. (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor Cell 64, 841-848 (Pubitemid 121001170)
14. Rapraeger, A. C., Krufka, A., and Olwin, B. B. (1991) Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation Science 252, 1705-1708 (Pubitemid 21917092)
15. Allen, B. L. and Rapraeger, A. C. (2003) Spatial and temporal expression of heparan sulfate in mouse development regulates FGF and FGF receptor assembly J. Cell Biol. 163, 637-648 (Pubitemid 37429875)
16. Mohammadi, M., Olsen, S. K., and Ibrahimi, O. A. (2005) Structural basis for fibroblast growth factor receptor activation Cytokine Growth Factor Rev. 16, 107-137 (Pubitemid 40616111)
17. Guimond, S., Maccarana, M., Olwin, B. B., Lindahl, U., and Rapraeger, A. C. (1993) Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4 J. Biol. Chem. 268, 23906-23914 (Pubitemid 23335365)
18. Ornitz, D. M., Yayon, A., Flanagan, J. G., Svahn, C. M., Levi, E., and Leder, P. (1992) Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells Mol. Cell. Biol. 12, 240-247
19. Okayama, M., Kimata, K., and Suzuki, S. (1973) The influence of p-nitrophenyl beta-d-xyloside on the synthesis of proteochondroitin sulfate by slices of embryonic chick cartilage J. Biochem. 74, 1069-1073
20. Yost, H. J. (1990) Inhibition of proteoglycan synthesis eliminates left-right asymmetry in Xenopus laevis cardiac looping Development 110, 865-874
21. Peal, D. S., Burns, C. G., Macrae, C. A., and Milan, D. (2009) Chondroitin sulfate expression is required for cardiac atrioventricular canal formation Dev. Dyn. 238, 3103-3110
22. Kuberan, B., Ethirajan, M., Victor, X. V., Tran, V., Nguyen, K., and Do, A. (2008) ″Click″ xylosides initiate glycosaminoglycan biosynthesis in a mammalian cell line ChemBioChem 9, 198-200 (Pubitemid 351196785)
23. Garud, D. R., Tran, V. M., Victor, X. V., Koketsu, M., and Kuberan, B. (2008) Inhibition of heparan sulfate and chondroitin sulfate proteoglycan biosynthesis J. Biol. Chem. 283, 28881-28887
24. Tran, V. M., Nguyen, T. K., Sorna, V., Loganathan, D., and Kuberan, B. (2013) Synthesis and assessment of glycosaminoglycan priming activity of cluster-xylosides for potential use as proteoglycan mimetics ACS Chem. Biol. 10.1021/cb300665u
25. Victor, X. V., Nguyen, T. K., Ethirajan, M., Tran, V. M., Nguyen, K. V., and Kuberan, B. (2009) Investigating the elusive mechanism of glycosaminoglycan biosynthesis J. Biol. Chem. 284, 25842-25853
26. Johnsson, R., Mani, K., and Ellervik, U. (2007) Synthesis and biology of bis-xylosylated dihydroxynaphthalenes Bioorg. Med. Chem. 15, 2868-2877 (Pubitemid 46402974)
27. Kelly, G. M., Erezyilmaz, D. F., and Moon, R. T. (1995) Induction of a secondary embryonic axis in zebrafish occurs following the overexpression of beta-catenin Mech. Dev. 53, 261-273
28. Furthauer, M., Van Celst, J., Thisse, C., and Thisse, B. (2004) Fgf signalling controls the dorsoventral patterning of the zebrafish embryo Development 131, 2853-2864 (Pubitemid 38997274)
29. Feldman, B., Gates, M. A., Egan, E. S., Dougan, S. T., Rennebeck, G., Sirotkin, H. I., Schier, A. F., and Talbot, W. S. (1998) Zebrafish organizer development and germ-layer formation require nodal-related signals Nature 395, 181-185 (Pubitemid 28425658)
30. Myers, D. C., Sepich, D. S., and Solnica-Krezel, L. (2002) Bmp activity gradient regulates convergent extension during zebrafish gastrulation Dev. Biol. 243, 81-98 (Pubitemid 34208405)
31. Tsang, M., Maegawa, S., Kiang, A., Habas, R., Weinberg, E., and Dawid, I. B. (2004) A role for MKP3 in axial patterning of the zebrafish embryo Development 131, 2769-2779 (Pubitemid 38997268)
32. Stachel, S. E., Grunwald, D. J., and Myers, P. Z. (1993) Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish Development 117, 1261-1274 (Pubitemid 23154492)
33. Dorsky, R. I., Sheldahl, L. C., and Moon, R. T. (2002) A transgenic Lef1/beta-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development Dev. Biol. 241, 229-237 (Pubitemid 34098688)
34. Nikaido, M., Tada, M., Saji, T., and Ueno, N. (1997) Conservation of BMP signaling in zebrafish mesoderm patterning Mech. Dev. 61, 75-88 (Pubitemid 27115944)
35. Onichtchouk, D., Chen, Y. G., Dosch, R., Gawantka, V., Delius, H., Massague, J., and Niehrs, C. (1999) Silencing of TGF-beta signalling by the pseudoreceptor BAMBI Nature 401, 480-485 (Pubitemid 29470206)
36. Meno, C., Ito, Y., Saijoh, Y., Matsuda, Y., Tashiro, K., Kuhara, S., and Hamada, H. (1997) Two closely-related left-right asymmetrically expressed genes, lefty-1 and lefty-2: their distinct expression domains, chromosomal linkage and direct neuralizing activity in Xenopus embryos Genes Cells 2, 513-524 (Pubitemid 127688599)
37. Sun, L., Tran, N., Tang, F., App, H., Hirth, P., McMahon, G., and Tang, C. (1998) Synthesis and biological evaluations of 3-substituted indolin-2-ones: a novel class of tyrosine kinase inhibitors that exhibit selectivity toward particular receptor tyrosine kinases J. Med. Chem. 41, 2588-2603 (Pubitemid 28321908)
38. Itoh, N. (2007) The Fgf families in humans, mice, and zebrafish: their evolutional processes and roles in development, metabolism, and disease Biol. Pharm. Bull. 30, 1819-1825 (Pubitemid 47607758)
39. Kudoh, T., Tsang, M., Hukriede, N. A., Chen, X., Dedekian, M., Clarke, C. J., Kiang, A., Schultz, S., Epstein, J. A., Toyama, R., and Dawid, I. B. (2001) A gene expression screen in zebrafish embryogenesis Genome Res. 11, 1979-1987 (Pubitemid 33138794)
40. Bao, X., Nishimura, S., Mikami, T., Yamada, S., Itoh, N., and Sugahara, K. (2004) Chondroitin sulfate/dermatan sulfate hybrid chains from embryonic pig brain, which contain a higher proportion of L-iduronic acid than those from adult pig brain, exhibit neuritogenic and growth factor binding activities J. Biol. Chem. 279, 9765-9776 (Pubitemid 38372574)
41. Nakamura, M., Uehara, Y., Asada, M., Honda, E., Nagai, N., Kimata, K., Suzuki, M., and Imamura, T. (2011) Sulfated glycosaminoglycans are required for specific and sensitive fibroblast growth factor (FGF) 19 signaling via FGF receptor 4 and betaKlotho J. Biol. Chem. 286, 26418-26423
42. Griffith, B. R., Allen, B. L., Rapraeger, A. C., and Kiessling, L. L. (2004) A polymer scaffold for protein oligomerization J. Am. Chem. Soc. 126, 1608-1609 (Pubitemid 38222731)
43. Rawat, M., Gama, C. I., Matson, J. B., and Hsieh-Wilson, L. C. (2008) Neuroactive chondroitin sulfate glycomimetics J. Am. Chem. Soc. 130, 2959-2961 (Pubitemid 351455965)
44. de Paz, J. L., Noti, C., Böhm, F., Werner, S., and Seeberger, P. H. (2007) Potentiation of fibroblast growth factor activity by synthetic heparin oligosaccharide glycodendrimers Chem. Biol. 14, 879-887 (Pubitemid 47268777)
45. Raman, R. and Sasisekharan, R. (2007) Cooperativity in Glycan-Protein Interactions Chem. Biol. 14, 873-874 (Pubitemid 47268787)
46. Westerfied, M. (2000) The Zebrafish Book. A guide for the laboratory use of zebrafish (Danio rerio), 4th ed., University of Oregon Press, Eugene, OR.
47. Schebesta, M., Lien, C. L., Engel, F. B., and Keating, M. T. (2006) Transcriptional profiling of caudal fin regeneration in zebrafish Sci. World J. 6 (Suppl 1) 38-54 (Pubitemid 46155752)
48. Thisse, C., Thisse, B., Schilling, T. F., and Postlethwait, J. H. (1993) Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos Development 119, 1203-1215 (Pubitemid 23358587)
49. Araki, I. and Brand, M. (2001) Morpholino-induced knockdown of fgf8 efficiently phenocopies the acerebellar (ace) phenotype Genesis 30, 157-159 (Pubitemid 32730764)