HSulf sulfatases catalyze processive and oriented 6-Odesulfation of heparan sulfate that differentially regulates fibroblast growth factor activity

FASEB Journal

Volumn 27, Issue 6, 2013, Pages 2431-2439

  Seffouh, Amal ^a   Milz, Fabian ^b   Przybylski, Cédric ^c   Laguri, Cédric ^a   Oosterhof, Arie ^d   Bourcier, Sébastien ^a   Sadir, Rabia ^a   Dutkowski, Elodie ^a   Daniel, Régis ^c   Van Kuppevelt, Toin H ^d   Dierks, Thomas ^b   Lortat Jacob, Hugues ^a   Vivès, Romain R ^a  

^a CNRS   (France)

^b BIELEFELD UNIVERSITY   (Germany)

^c UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Enzymatic mechanism; Glycosaminoglycan; Interaction; Proteoglycan; Structure function relationships

Indexed keywords

CARBOHYDRATE; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; HEPARAN SULFATE; HSULF 2 SULFATASE; OCTASACCHARIDE; OLIGOSACCHARIDE; SULFATASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANALYTIC METHOD; ANIMAL CELL; ARTICLE; CATALYSIS; CELL SURFACE; CONTROLLED STUDY; DESULFATION; ENZYME ACTIVITY; ENZYME STRUCTURE; FLUORESCENCE ACTIVATED CELL SORTING; MASS SPECTROMETRY; MITOGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEIN PURIFICATION; SULFATION;

ENZYMATIC MECHANISM; GLYCOSAMINOGLYCAN; INTERACTION; PROTEOGLYCAN; STRUCTURE/FUNCTION RELATIONSHIPS;

CATALYSIS; CELL LINE; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; HEPARITIN SULFATE; HUMANS; OLIGOSACCHARIDES; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBSTRATE SPECIFICITY; SULFOTRANSFERASES;

EID: 84878760333     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-226373     Document Type: Article

References (37)

1. Sarrazin, S., Lamanna, W. C., and Esko, J. D. (2011) Heparan sulfate proteoglycans. Cold Spring Harb. Perspect. Biol. 3, a0049522
2. Lortat-Jacob, H. (2009) The molecular basis and functional implications of chemokine interactions with heparan sulphate. Curr. Opin. Struct. Biol. 19, 543-5488
3. Ori, A., Wilkinson, M. C., and Fernig, D. G. (2008) The heparanome and regulation of cell function: structures, functions and challenges. Front. Biosci. 13, 4309-43388
4. Lindahl, U., and Li, J. P. (2009) Interactions between heparan sulfate and proteins-design and functional implications. Int. Rev. Cell Mol. Biol. 276, 105-1599
5. Esko, J. D., and Selleck, S. B. (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-4711
6. Dhoot, G. K., Gustafsson, M. K., Ai, X., Sun, W., Standiford, D. M., and Emerson, C. P., Jr. (2001) Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293, 1663-16666
7. Ohto, T., Uchida, H., Yamazaki, H., Keino-Masu, K., Matsui, A., and Masu, M. (2002) Identification of a novel nonlysosomal sulphatase expressed in the floor plate, choroid plexus and cartilage. Genes Cells 7, 173-1855
8. Morimoto-Tomita, M., Uchimura, K., Werb, Z., Hemmerich, S., and Rosen, S. D. (2002) Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J. Biol. Chem. 277, 49175-491855
9. Ai, X., Do, A. T., Lozynska, O., Kusche-Gullberg, M., Lindahl, U., and Emerson, C. P., Jr. (2003) QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J. Cell Biol. 162, 341-3511
10. Viviano, B. L., Paine-Saunders, S., Gasiunas, N., Gallagher, J., and Saunders, S. (2004) Domain-specific modification of heparan sulfate by Qsulf1 modulates the binding of the bone morphogenetic protein antagonist Noggin. J. Biol. Chem. 279, 5604-56111
11. Uchimura, K., Morimoto-Tomita, M., Bistrup, A., Li, J., Lyon, M., Gallagher, J., Werb, Z., and Rosen, S. D. (2006) 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. 7, 22
12. Lamanna, W. C., Baldwin, R. J., Padva, M., Kalus, I., Ten Dam, G., van Kuppevelt, T. H., Gallagher, J. T., von Figura, K., Dierks, T., and Merry, C. L. (2006) Heparan sulfate 6-O-endosulfatases: discrete in vivo activities and functional co-operativity. Biochem. J. 400, 63-733
13. Lum, D. H., Tan, J., Rosen, S. D., and Werb, Z. (2007) Gene trap disruption of the mouse heparan sulfate 6-O-endosulfatase gene, Sulf2. Mol. Cell. Biol. 27, 678-6888
14. Freeman, S. D., Moore, W. M., Guiral, E. C., Holme, A. D., Turnbull, J. E., and Pownall, M. E. (2008) Extracellular regulation of developmental cell signaling by XtSulf1. Dev. Biol. 320, 436-4455
15. Kalus, I., Salmen, B., Viebahn, C., von Figura, K., Schmitz, D., D'Hooge, R., and Dierks, T. (2009) Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity. J. Cell. Mol. Med. 13, 4505-45211
16. Narita, K., Staub, J., Chien, J., Meyer, K., Bauer, M., Friedl, A., Ramakrishnan, S., and Shridhar, V. (2006) HSulf-1 inhibits angiogenesis and tumorigenesis in vivo. Cancer Res. 66, 6025-60322
17. Nawroth, R., van Zante, A., Cervantes, S., McManus, M., Hebrok, M., and Rosen, S. D. (2007) Extracellular sulfatases, elements of the Wnt signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells. PLoS One 2, e3922
18. Lemjabbar-Alaoui, H., van Zante, A., Singer, M. S., Xue, Q., Wang, Y. Q., Tsay, D., He, B., Jablons, D. M., and Rosen, S. D. (2009) Sulf-2, a heparan sulfate endosulfatase, promotes human lung carcinogenesis. Oncogene 29, 635-6466
19. Dai, Y., Yang, Y., MacLeod, V., Yue, X., Rapraeger, A. C., Shriver, Z., Venkataraman, G., Sasisekharan, R., and Sanderson, R. D. (2005) HSulf-1 and HSulf-2 are potent inhibitors of myeloma tumor growth in vivo. J. Biol. Chem. 280, 40066-400733
20. Rosen, S. D., and Lemjabbar-Alaoui, H. (2010) Sulf-2: an extracellular modulator of cell signaling and a cancer target candidate. Expert Opin. Ther. Targets 14, 935-9499
21. Chabrol, E., Nurisso, A., Daina, A., Vassal-Stermann, E., Thepaut, M., Girard, E., Vives, R. R., and Fieschi, F. (2012) Glycosaminoglycans are interactants of langerin: comparison with gp120 highlights an unexpected calcium-independent binding mode. PLoS One 7, e507222
22. Pye, D. A., Vives, R. R., Turnbull, J. E., Hyde, P., and Gallagher, J. T. (1998) Heparan sulfate oligosaccharides require 6-Osulfation for promotion of basic fibroblast growth factor mitogenic activity. J. Biol. Chem. 273, 22936-229422
23. Przybylski, C., Gonnet, F., Bonnaffe, D., Hersant, Y., Lortat- Jacob, H., and Daniel, R. (2010) HABA-based ionic liquid matrices for UV-MALDI-MS analysis of heparin and heparan sulfate oligosaccharides. Glycobiology 20, 224-2344
24. Vives, R. R., Pye, D. A., Salmivirta, M., Hopwood, J. J., Lindahl, U., and Gallagher, J. T. (1999) Sequence analysis of heparan sulphate and heparin oligosaccharides. Biochem. J. 339, 767-7733
25. Frese, M. A., Milz, F., Dick, M., Lamanna, W. C., and Dierks, T. (2009) Characterization of the human sulfatase Sulf1 and its high affinity heparin/heparan sulfate interaction domain. J. Biol. Chem. 284, 28033-280444
26. Pempe, E. H., Burch, T. C., Law, C. J., and Liu, J. (2012) Substrate specificity of 6-O-endosulfatase (Sulf-2) and its implications in synthesizing anticoagulant heparan sulfate. Glycobiology 22, 1353-13622
27. Lamanna, W. C., Frese, M. A., Balleininger, M., and Dierks, T. (2008) Sulf loss influences N-, 2-O-, and 6-O-sulfation of multiple heparan sulfate proteoglycans and modulates fibroblast growth factor signaling. J. Biol. Chem. 283, 27724-277355
28. Staples, G. O., Shi, X., and Zaia, J. (2011) Glycomics analysis of mammalian heparan sulfates modified by the human extracellular sulfatase HSulf2. PLoS One 6, e166899
29. Capila, I., and Linhardt, R. J. (2002) Heparin-protein interactions. Angew. Chem. Int. Ed. Engl. 41, 391-4122
30. Yates, E. A., Santini, F., Guerrini, M., Naggi, A., Torri, G., and Casu, B. (1996) 1H and 13C NMR spectral assignments of the major sequences of twelve systematically modified heparin derivatives. Carbohydr. Res. 294, 15-277
31. 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, 23906-239144
32. Ishihara, M., Takano, R., Kanda, T., Hayashi, K., Hara, S., Kikuchi, H., and Yoshida, K. (1995) Importance of 6-O-sulfate groups of glucosamine residues in heparin for activation of FGF-1 and FGF-2. J. Biochem. Tokyo 118, 1255-12600
33. Pye, D. A., Vives, R. R., Hyde, P., and Gallagher, J. T. (2000) Regulation of FGF-1 mitogenic activity by heparan sulfate oligosaccharides is dependent on specific structural features: differential requirements for the modulation of FGF-1 and FGF-2. Glycobiology 10, 1183-11922
34. Jemth, P., Kreuger, J., Kusche-Gullberg, M., Sturiale, L., Gimenez- Gallego, G., and Lindahl, U. (2002) Biosynthetic oligosaccharide libraries for identification of protein-binding heparan sulfate motifs. Exploring the structural diversity by screening for FGF1 and FGF2 binding. J. Biol. Chem. 277, 30567-305733
35. Hossain, M. M., Hosono-Fukao, T., Tang, R., Sugaya, N., van Kuppevelt, T. H., Jenniskens, G. J., Kimata, K., Rosen, S. D., and Uchimura, K. (2010) Direct detection of HSulf-1 and HSulf-2 activities on extracellular heparan sulfate and their inhibition by PI-88. Glycobiology 20, 175-1866
36. Kudchadkar, R., Gonzalez, R., and Lewis, K. D. (2008) PI-88: a novel inhibitor of angiogenesis. Expert Opin. Investig. Drugs 17, 1769-17766
37. Morimoto-Tomita, M., Uchimura, K., Bistrup, A., Lum, D. H., Egeblad, M., Boudreau, N., Werb, Z., and Rosen, S. D. (2005) Sulf-2, a proangiogenic heparan sulfate endosulfatase, is upregulated in breast cancer. Neoplasia 7, 1001-10100