Chondroitin Sulfate Lyases: Applications in Analysis and Glycobiology

Advances in Pharmacology

Volumn 53, Issue , 2006, Pages 167-186

  Petit, Emmanuel ^a   Delattre, Cedric ^b   Papy Garcia, Dulce ^c   Michaud, Philippe ^d  

^a OTR3 SAS   (France)

^b EPMV   (France)

^c Université Paris 12 Val de Marne ^*  (France)

^d UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN ABC LYASE; CHONDROITIN SULFATE; DERMATAN SULFATE;

ANIMAL; CHEMISTRY; HUMAN; PHYSIOLOGY; REVIEW;

ANIMALS; CHONDROITIN ABC LYASE; CHONDROITIN LYASES; CHONDROITIN SULFATES; DERMATAN SULFATE; HUMANS;

EID: 33846247156     PISSN: 10543589     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1054-3589(05)53008-4     Document Type: Review

References (88)

1. Al-Hakim A., and Linhardt R.J. Capillary electrophoresis for the analysis of chondroitin sulfate and dermatan sulfate derived disaccharides. Anal. Biochem. 195 (1991) 68-73
2. Avci F.Y., Toida T., and Linhardt R.J. Chondroitin O-methyl ester: An unusual substrate for chondroitin AC lyase. Carbohyd. Polym. 338 (2003) 2101-2104
3. Bellamy W.R. A novel Bacillus sp. capable of degrading sulfated glycosaminoglycans. In: Horikoshi K., and Grant W.D. (Eds). "Superbugs, Microorganisms in Extreme Environments" (1990), Japan Scientific Societies Press, Tokyo 143-157
4. Bradbury E.J., Moon L.D.F., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., and McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416 (2002) 636-640
5. Brakebusch C., Seidenbecher C.I., Asztely F., Rauch U., Matthies H., Meyer H., Krug M., Bockers T.M., Zhou X., Kreutz M.R., Montag D., Gundelfinger E.D., et al. Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol. Cell. Biol. 22 (2002) 7417-7427
6. Bukalo O., Schachner M., and Dityatev A. Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104 (2001) 359-369
7. Capila I., Wu Y., Rethwisch D.W., Matte A., Cygler M., and Linhardt R.J. Role of arginine 292 in the catalytic activity of chondroitin AC lyase from Flavobacterium heparinum. Biochim. Biophys. Acta 1597 (2002) 260-270
8. Clement A.M., Nadanaka S., Masayama K., Mandl C., Sugahara K., and Faissner A. The DSD-1 carbohydrate epitope depends on sulfation, correlates with chondroitin sulfate D motifs, and is sufficient to promote neurite outgrowth. J. Biol. Chem. 273 (1998) 28444-28453
9. Coutinho P.M., and Henrissat B. Carbohydrate-active enzymes: An integrated database approach. In: Gilbert H.J., Davies G., Henrissat B., and Svensson B. (Eds). "Recent Advances in Carbohydrate Bioengineering" (1999), The Royal Society of Chemistry, Cambridge 3-12
10. Dai Y., Whittal R.M., Bridges C.A., Isogai Y., Hindsgaul O., and Li L. Matrix-assisted laser desorption ionization mass spectrometry for the analysis of monosulfated oligosaccharides. Carbohyd. Res. 304 (1997) 1-9
11. Ernst S., Langer R., Cooney C.L., and Sasisekharan R. Enzymic degradation of glycosaminoglycans. Crit. Rev. Biochem. Mol. 30 (1995) 387-444
12. Feizi T., and Chai W. Oligosaccharide microarrays to decipher the glyco code. Nat. Rev. Mol. Cell. Biol. 5 (2004) 582-588
13. Féthière J., Eggimann B., and Cygler M. Crystal structure of chondroitin AC lyase, a representative of a family of glycosaminoglycan degrading enzymes. J. Mol. Biol. 288 (1999) 635-647
14. Fraser P.E., Darabie A.A., and McLaurin J.A. Amyloid-beta interactions with chondroitin sulfate-derived monosaccharides and disaccharides: Implications for drug development. J. Biol. Chem. 276 (2001) 6412-6419
15. Gu K., Linhardt R.J., Laliberte M., Gu K., and Zimmermann J. Purification, characterization and specificity of chondroitin lyases and glycuronidase from Flavobacterium heparinum. Biochem. J. 312 (1995) 569-577
16. Gu K., Liu J., Pervin A., and Linhardt R.J. Comparison of the activity of two chondroitin AC lyases on dermatan sulfate. Carbohyd. Res. 244 (1993) 369-377
17. Hamai A., Hashimoto N., Mochizuki H., Kato F., Makiguchi Y., Horie K., and Suzuki S. Two distinct chondroitin sulfate ABC lyases: An endoeliminase yielding tetrasaccharides and an exoeliminase preferentially acting on oligosaccharides. J. Biol. Chem. 272 14 (1997) 9123-9130
18. Hanson S., Best M., Bryan M.C., and Wong C.H. Chemoenzymatic synthesis of oligosaccharides and glycoproteins. Trends Biochem. Sci. 29 (2004) 656-663
19. Hernaiz M.J., and Linhardt R.J. Degradation of chondroitin sulfate and dermatan sulfate with chondroitin lyases. Methods Mol. Biol. 171 (2001) 363-371
20. 2+ Binding to Pectate Lyase C. J. Biol. Chem. 278 (2003) 12271-12277
21. Hiyama K., and Okada S. Action of chondroitinases I. J. Biochem. 80 (1976) 1201-1207
22. Hiyama K., and Okada S. Action of chondroitinases III. J. Biochem. 82 (1977) 429-436
23. Hong S.W., Kim B.T., Shin H.Y., Kim W.S., Lee K.S., Kim Y.S., and Kim D.H. Purification and characterization of novel chondroitin ABC and AC lyases from Bacteroides stercoris HJ-15, a human intestinal anaerobic bacterium. Eur. J. Biochem. 269 (2002) 2934-2940
24. Huang W., Boju L., Tkalec L., Su H., Yang H.O., Gunay N.S., Linhardt R.J., Kim Y.S., Matte A., and Cygler M. Active site of chondroitin AC lyase revealed by the structure of enzyme-oligosaccharide complexes and mutagenesis. Biochemistry 40 (2001) 2359-2372
25. Huang W., Lunin V.V., Li Y., Suzuki S., Sugiura N., Miyazono H., and Cygler. M. Crystal structure of Proteus vulgaris chondroitin sulfate ABC lyase I at 1.9 A resolution. J. Mol. Biol. 328 (2003) 623-634
26. Huang W., Matte A., Li Y., Kim Y.S., Linhardt R.J., Su H., and Cygler M. Crystal structure of chondroitinase B from Flavobacterium heparinum and its complex with a disaccharide product at 1.7 Å resolution. J. Mol. Biol. 294 (1999) 1257-1269
27. 13C-NMR studies of reduced disaccharides and tetrasaccharides. Eur. J. Biochem. 268 (2001) 1181-1189
28. Hwang H.Y., Olsen S.K., Esko J.D., and Horvitz H.R. Caenorhabditis elegans early embryogenesis and vulval morphogenesis depend on chondroitin biosynthesis. Nature 423 (2003) 439-443
29. Imanari T., Toida T., Koshiishi I., and Toyoda H. High performance liquid chromatographic analysis of glycosaminoglycans derived oligosaccharides. J. Chromatogr. A 720 (1996) 275-293
30. Jandik K.A., Gu K., and Linhardt R.J. Action patterns of polysaccharide lyases on glycosaminoglycans. Glycobiology 4 (1994) 286-296
31. Jedrzejas M.J., Mello L.V., De Groot B.L., and Li S. Mechanism of hyaluronan degradation by Streptococcus pneumoniae hyaluronate lyase: Structures of complexes with the substrate. J. Biol. Chem. 277 (2002) 28287-28297
32. Juhasz P., and Biemann K. Utility of non-covalent complexes in the matrix-assisted laser desorption ionization mass spectrometry of heparin-derived oligosaccharides. Carbohydr. Res. 270 (1995) 131-147
33. Karamanos N.K., Vanky P., Syrokou A., and Hjerpe A. Identity of dermatan and chondroitin sequences in dermatan sulfate chains by using fragmentation with chondroitinases and ion pair high performance liquid chromatography. Anal. Biochem. 225 (1995) 220-230
34. Karst N.A., and Linhardt R.J. Recent chemical and enzymatic approaches to the synthesis of glycosaminoglycan oligosaccharides. Curr. Med. Chem. 10 (2003) 1993-2031
35. Katz H.R., Austen K.F., Caterson B., and Stevens R.L. Secretory granules of heparin-containing rat serosal mast cells also possess highly sulfated chondroitin sulfate proteoglycans. J. Biol. Chem. 261 (1986) 13393-13396
36. Kawashima H., Atarashi K., Hirose M., Hirose J., Yamada S., Sugahara K., and Miyasaka M. Oversulfated chondroitin/dermatan sulfates containing GlcAbeta1/IdoAalpha1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. J. Biol. Chem. 277 (2002) 12921-12930
37. Kinoshita A., Yamada S., Haslam S.M., Morris H.R., Dell A., and Sugahara K. Novel tetrasaccharides isolated from squid cartilage chondroitin sulfate E contain unusual sulfated disaccharide units GlcA(3-O-sulfate)β1-3GalNAc(6-O-sulfate) or GlcA(3-O-sulfate)β1-3GalNAc(4,6-O-disulfate). J. Biol. Chem. 272 (1997) 19656-19665
38. Kinoshita-Toyoda A., Yamada S., Haslam S.M., Khoo K.H., Sugiura M., Morris H.R., Dell A., and Sugahara K. Structural determination of five novel tetrasaccharides containing 3-O-sulfated D-glucuronic acid and two rare oligosaccharides containing a beta-D-glucose branch isolated from squid cartilage chondroitin sulfate E. Biochemistry 43 (2004) 11063-11074
39. Kitagawa H., Tanaka Y., Yamada S., Seno N., Haslam S.M., Morris H.R., Dell A., and Sugahara K. A novel pentasaccharide sequence GlcA(3-sulfate)(β1-3)GalNAc(4-sulfate)(β1-4)(Fucα1-3)Glc A(β1-3)GalNAc(4-sulfate) in the oligosaccharides isolated from king crab cartilage chondroitin sulfate K and its differential susceptibility to chondroitinases and hyaluronidase. Biochemistry 36 (1997) 3998-4008
40. Kitamikado M., and Lee Y.-Z. Chondroitinase-producing bacteria in natural habitats. Appl. Microbiol. 29 (1975) 414-421
41. Kobayashi S., Oguri K., Yaoita E., Kobayashi K., and Okayama M. Highly sulfated proteochondroitin sulfates synthesized in vitro by rat glomeruli. Biochim. Biophys. Acta 841 (1985) 71-80
42. Lamari F.N., Kuhn R., and Karamanos N.K. Derivatization of carbohydrates for chromatographic, electrophoretic and mass spectrometric structure analysis. J. Chromatogr. B 793 (2003) 15-36
43. Lauder R.M., Huckerby T.N., Brown G.M., Bayliss M.T., and Nieduszynski I.A. Age-related changes in the sulphation of the chondroitin sulphate linkage region from human articular cartilage aggrecan. Biochem. J. 358 (2001) 523-528
44. Lechner J. Structure and biosynthesis of prokaryotic glycoproteins. Annu. Rev. Biochem. 60 (1989) 443-475
45. Li S., and Jedrzejas M.J. Hyaluronan binding and degradation by Streptococcus agalactiae hyaluronate lyase. J. Biol. Chem. 276 (2001) 41407-41416
46. Li S., Kelly S.J., Lamani E., Ferraroni M., and Jedrzejas M.J. Structural basis of hyaluronan degradation by Streptococcus pneumoniae hyaluronate lyase. EMBO J. 19 (2000) 1228-1240
47. Liu D., Shriver Z., Godavarti R., Venkataraman G., and Sasisekharan R. The calcium-binding sites of heparinase I from Flavobacterium heparinum are essential for enzymatic activity. J. Biol. Chem. 274 (1999) 4089-4095
48. Lunin V.V., Li Y., Linhardt R.J., Miyazono H., Kyogashima M., Kaneko T., Bell A.W., and Cygler M. High-resolution crystal structure of Arthrobacter aurescens chondroitin AC lyase: An enzyme-substrate complex defines the catalytic mechanism. J. Mol. Biol. 337 (2004) 367-386
49. Michaud P., Da Costa A., Courtois B., and Courtois J. Polysaccharides Lyases: Recent developments as biotechnological tools. Crit. Rev. Biotechnol. 23 (2003) 233-266
50. Michel G., Pojasek K., Li Y., Sulea T., Linhardt R.J., Raman R., Prabhakar V., Sasisekharan R., and Cygler M. The structure of chondroitin B lyase complexed with glycosaminoglycan oligosaccharides unravels a calcium-dependent catalytic machinery. J. Biol. Chem. 279 (2004) 32882-32896
51. Moon L.D.F., Asher R.A., Rhodes K.E., and Fawcett J.W. Regeneration of CNS axons back to their original target following treatment of adult rat brain with chondroitinase ABC. Nat. Neurosci. 4 (2001) 465-466
52. Nadanaka S., Clement A., Masayama K., Faissner A., and Sugahara K. Characteristic hexasaccharide sequences in octasaccharides derived from shark cartilage chondroitin sulfate D with a neurite outgrowth promoting activity. J. Biol. Chem. 273 (1998) 3296-3307
53. Nandini C.D., Mikami T., Ohta M., Itoh N., Akiyama-Nambu F., and Sugahara K. 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 (2004) 50799-50809
54. Ohhashi Y., Hasumi F., and Mori Y. Comparative study on glycosaminoglycans synthesized in peripheral and peritoneal polymorphonuclear leucocytes from guinea pigs. Biochem. J. 217 (1984) 199-207
55. Ototani N., and Yosizawa Z. Purification of chondroitinase B and chondroitinase C using glycosaminoglycan-bound AH-Sepharose 4B. Carbohydr. Res. 70 (1979) 295-306
56. Park S., Lee M.R., Pyo S.J., and Shin I. Carbohydrate chips for studying high-throughput carbohydrate-protein interactions. J. Am. Chem. Soc. 126 (2004) 4812-4819
57. Penc S.F., Pomahac B., Winkler T., Dorschner R.A., Eriksson E., Herndon M., and Gallo R.L. Dermatan sulfate released after injury is a potent promoter of fibroblast growth factor-2 function. J. Biol. Chem. 273 (1998) 28116-28121
58. Perugino G., Trincone A., Rossi M., and Moracci M. Oligosaccharide synthesis by glycosynthases. Trends Biotechnol. 22 (2004) 31-37
59. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J.W., and Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298 (2002) 1248-1251 See commentary
60. Fox K., and Caterson B. Freeing the brain from the perineuronal net. Science 298 (2002) 1187-1189
61. Pojasek K., Raman R., Kiley P., and Venkataraman G. Biochemical characterization of the chondroitinase B active site. J. Biol. Chem. 277 34 (2002) 31179-31186
62. Ponnuraj K., and Jedrzejas M.J. Mechanism of hyaluronan binding and degradation: Structure of Streptococcus pneumoniae hyaluronate lyase in complex with hyaluronic acid disaccharide at 1.7 A resolution. J. Mol. Biol. 299 (2000) 885-895
63. Prabhakar V., Capila I., Bosques C.J., Pojasek K., and Sasisekharan R. Chondroitinase ABC I from Proteus vulgaris: Cloning, recombinant expression and active site identification. Biochem. J. 386 1 (2005) 103-112
64. Rhodes K.E., and Fawcett J.W. Chondroitin sulphate proteoglycans: Preventing plasticity or protecting the CNS?. J. Anat. 204 (2004) 33-48
65. Sato N., Shimada M., Nakajima H., Oda H., and Kimura S. Cloning and expression in Escherichia coli of the gene encoding the Proteus vulgaris chondroitin ABC lyase. Appl. Microbiol. Biotechnol. 41 (1994) 39-46
66. Schiller J., Arnhold J., Benard S., Reichl S., and Arnold K. Cartilage degradation by hyaluronate lyase and chondroitin ABC lyase: A MALDI-TOF mass spectrometric study. Carbohydr. Res. 318 (1999) 116-122
67. Stringer-Roth K.M., Yunghans W., and Caslake L.F. Differences in chondroitin AC lyase activity of Flavobacterium columnare isolates. J. Fish Dis. 25 (2002) 687-691
68. Sugahara K., Mikami T., Uyama T., Mizuguchi S., Nomura K., and Kitagawa H. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 13 (2003) 612-620
69. Sugahara K., Nadanaka S., Takeda K., and Kojima T. Structural analysis of unsaturated hexasaccharides isolated from shark cartilage chondroitin sulfate D that are substrates for the exolytic action of chondroitin ABC lyase. Eur. J. Biochem. 239 (1996) 871-880
70. Sugahara K., Takemura Y., Sugiura M., Kohno Y., Yoshida K., Takeda K., Khoo K.H., Morris H.R., and Dell A. Chondroitinase ABC-resistant sulfated trisaccharides isolated from digests of chondroitin/dermatan sulfate chains. Carbohydr. Res. 255 (1994) 165-182
71. Takagaki K., Munakata H., Kakizaki I., Iwafune M., Itabashi T., and Endo M. Domain structure of chondroitin sulfate E octasaccharides binding to type V collagen. J. Biol. Chem. 277 (2002) 8882-8889
72. Takegawa K., Iwahara K., and Iwahara S. Purification and properties of chondroitinase produced by a bacterium isolated from soil. J. Ferment. Bioeng. 72 (1991) 128-131
73. Tanaka M., Maeda N., Noda M., and Marunouchi T. A chondroitin sulfate proteoglycan PTPζ/RPTPβ regulates the morphogenesis of Purkinje cell dendrites in the developing cerebellum. J. Neurosci. 23 (2003) 2804-2814
74. Tatemoto H., Muto N., Yim S.D., and Nakada T. Anti-hyaluronidase oligosaccharide derived from chondroitin sulfate a effectively reduces polyspermy during in vitro fertilization of porcine oocytes. Biol. Reprod. 72 (2005) 127-134
75. Tkalec A.L., Fink D., Blain F., Zhang-Sun G., Laliberte M., Bennett D.C., Gu K., Zimmermann J.J., and Su H. Isolation and expression in Escherichia coli of cslA and cslB, genes coding for the chondroitin sulfate-degrading enzymes chondroitinase AC and chondroitinase B, respectively, from Flavobacterium heparinum. Appl. Envron. Microbiol. 66 (2000) 29-35
76. Tollefsen D.M., Peacock M.E., and Monafo W.J. Molecular size of dermatan sulfate oligosaccharides required to bind and activate heparin cofactor II. J. Biol. Chem. 261 (1986) 8854-8858
77. Tropea D., Caleo M., and Maffei L. Synergistic effects of brain-derived neurotrophic factor and chondroitinase ABC on retinal fiber sprouting after denervation of the superior colliculus in adult rats. J. Neurosci. 23 (2003) 7034-7044
78. Ueoka C., Nadanaka S., Seno N., Khoo K.H., and Sugahara K. Structural determination of novel tetra- and hexasaccharide sequences isolated from chondroitin sulfate H (oversulfated dermatan sulfate) of hagfish notochord. Glycoconj. J. 16 (1999) 291-305
79. Uhlin-Hansen L., Eskeland T., and Kolset S.O. Modulation of the expression of chondroitin sulfate proteoglycan in stimulated human monocytes. J. Biol. Chem. 264 (1989) 14916-14922
80. Werz D.B., and Seeberger P.H. Carbohydrates as the next frontier in pharmaceutical research. Chemistry 11 (2005) 3194-3206
81. Yang H.O., Gunay N.S., Toida T., Kuberan B., Yu G., Kim Y.S., and Linhardt R.J. Preparation and structural determination of dermatan sulfate-derived oligosaccharides. Glycobiology 10 (2000) 1033-1039
82. Yaoita E., Oguri K., Okayama E., Kawasaki K., Kobayashi S., Kihara I., and Okayama M. Isolation and characterization of proteoglycans synthesized by cultured mesangial cells. J. Biol. Chem. 265 (1990) 522-531
83. Zaia J., and Costello C.E. Compositional analysis of glycosaminoglycans by electrospray mass spectrometry. Anal. Chem. 73 (2001) 233-239
84. Zamfir A., Seidler D.G., Kresse H., and Peter-Katalinic J. Structural investigation of chondroitin/dermatan sulfate oligosaccharides from human skin fibroblast decorin. Glycobiology 11 (2003) 733-742
85. Zamfir A., Seidler D.G., Kresse H., and Peter-Katalinic J. Structural characterization of chondroitin/dermatan sulfate oligosaccharides from bovine aorta by capillary electrophoresis and electrospray ionization quadrupole time-of-flight tandem mass spectrometry. Rapid Commun. Mass Spectrom. 16 (2002) 2015-2024
86. Zhou X.H., Brakebusch C., Matthies H., Oohashi T., Hirsch E., Moser M., Krug M., Seidenbecher C.I., Boeckers T.M., Rauch U., Buettner R., Gundelfinger E.D., et al. Neurocan is dispensable for brain development. Mol. Cell. Biol. 21 (2001) 5970-5978
87. Zou P., Zou K., Muramatsu H., Ichihara-Tanaka K., Habuchi O., Ohtake S., Ikematsu S., Sakuma S., and Muramatsu T. Glycosaminoglycan structures required for strong binding to midkine, a heparin-binding growth factor. Glycobiology 13 (2003) 35-42
88. Zuo J., Neubauer D., Graham J., Krekoski C.A., Ferguson T.A., and Muir D. Regeneration of axons after nerve transection repair is enhanced by degradation of chondroitin sulfate proteoglycan. Exp. Neurol. 176 (2002) 221-228