Composite active site of chondroitin lyase ABC accepting both epimers of uronic acid

Glycobiology

Volumn 18, Issue 3, 2008, Pages 270-277

  Shaya, D ^a   Hahn, Bum Soo ^b   Bjerkan, Tonje Marita ^c   Kim, Wan Seok ^d   Park, Nam Young ^e   Sim, Joon Soo ^e   Kim, Yeong Shik ^e   Cygler, Mirek ^a,f  

^a MCGILL UNIVERSITY   (Canada)

^b National Institute of Animal Science   (South Korea)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d The Catholic University of Korea   (South Korea)

^e Seoul National University   (South Korea)

^f NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Catalytic mechanism; Chondroitinase ABC; Crystal structure; Glycosaminoglycans; Site directed mutagenesis

Indexed keywords

CALCIUM ION; CHONDROITIN ABC LYASE; CHONDROITIN SULFATE; DERMATAN SULFATE; GLUCURONIC ACID; IDURONIC ACID; MAGNESIUM ION; TETRAPEPTIDE; URONIC ACID;

ARTICLE; BACTEROIDES THETAIOTAOMICRON; BINDING SITE; CARBOHYDRATE METABOLISM; CATALYSIS; CLUSTER ANALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME DEGRADATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; EPIMER; NONHUMAN; PRIORITY JOURNAL; PROTEUS VULGARIS; STRUCTURE ANALYSIS;

BACTEROIDES; BINDING SITES; CARBOHYDRATE CONFORMATION; CATALYSIS; CHONDROITIN ABC LYASE; CHONDROITIN SULFATES; DERMATAN SULFATE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; URONIC ACIDS;

BACTERIA (MICROORGANISMS); BACTEROIDES THETAIOTAOMICRON; PROTEUS VULGARIS;

EID: 40649115280     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwn002     Document Type: Article

References (46)

1. Allard ST, Giraud MF, Naismith JH. 2001. Epimerases: Structure, function and mechanism. Cell Mol Life Sci. 58:1650-1665.
2. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Host-bacterial mutualism in the human intestine. Science. 307:1915-1920.
3. Bao X, Nishimura S, Mikami T, Yamada S, Itoh N, 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.
4. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. 2000. The protein data bank. Nucleic Acids Res. 28:235-242.
5. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 68:729-777.
6. Bricogne G, Vonrhein C, Flensburg C, Schiltz M, Paciorek W. 2003. Generation, representation and flow of phase information in structure determination: Recent developments in and around SHARP 2.0. Acta Crystallogr, Sect D: Biol Crystallogr. 59:2023-2030.
7. Capila I, Wu Y, Rethwisch DW, Matte A, Cygler M, Linhardt RJ. 2002. Role of arginine 292 in the catalytic activity of chondroitin AC lyase from Flavobacterium heparinum. Biochim Biophys Acta. 1597:260-270.
8. Carvalho AL, Goyal A, Prates JA, Bolam DN, Gilbert HJ, Pires VM, Ferreira LM, Planas A, Romao MJ, Fontes CM. 2004. The family 11 carbohydrate-binding module of Clostridium thermocellum Lic26A-Ce15E accommodates beta-1,4- and beta-1,3-1,4-mixed linked glucans at a single binding site. J Biol Chem. 279:34785-34793.
9. Charnock SJ, Bolam DN, Turkenburg JP, Gilbert HJ, Ferreira LM, Davies GJ, Fontes CM. 2000. ne X6 "thermostabilizing" domains of xylanases are carbohydrate-binding modules: Structure and biochemistry of the Clostridium thermocellum X6b domain. Biochemistry. 39:5013-5021.
10. D'Amore PA. 1990. Modes of FGF release in vivo and in vitro. Cancer Metastasis Rev. 9:227-238.
11. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr, Sect D: Biol Crystallogr. 60:2126-2132.
12. Ernst S, Langer R, Cooney CL, Sasisekharan R. 1995. Enzymatic degradation of glycosaminoglycans. Crit Rev Biochem Mol Biol. 30:387-444.
13. Féthière J, Eggimann B, Cygler M. 1999. Crystal structure of chondroitin AC lyase, a representative of a family of glycosaminoglycan degrading enzymes. J Mol Biol. 288:635-647.
14. Folkman J, Klagsbrun M. 1987. Angiogenic factors. Science. 235:442-447.
15. Gacesa P. 1987. Alginate-modifying enzymes. A proposed unified mechanism of action for the lyases and epimerases. FEBS Lett. 212:199-202.
16. Hamai A, Hashimoto N, Mochizuki H, Kato F, Makiguchi Y, Horie K, Suzuki S. 1997. Two distinct chondroitin sulfate ABC lyases. An endoeliminase yielding tetrasaccharides and an exoeliminase preferentially acting on oligosaccharides. J Biol Chem. 272:9123-9130.
17. Hashimoto W, Nankai H, Mikami B, Murata K. 2003. Crystal structure of Bacillus sp. GL1 xanthan lyase, which acts on the side chains of xanthan. J Biol Chem. 278:7663-7673.
18. Hendrickson WA, Horton JR, LeMaster DM. 1990. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): A vehicle for direct determination of three-dimensional structure. EMBO J. 9:1665-1672.
19. 2+ binding to pectate Iyase C. J Biol Chem. 278:12271-12277.
20. Huang W, Boju L, Tkalec L, Su H, Yang HO, Gunay NS, Linhardt RJ, Kim YS, Matte A, Cygler M. 2001. Active site of chondroitin AC lyase revealed by the structure of enzyme-oligosaccharide complexes and mutagenesis. Biochemistry. 40:2359-2372.
21. Huang W, Lunin VV, Li Y, Suzuki S, Sugiura N, Miyazono H, Cygler M. 2003. Crystal structure of Proteus vulgaris chondroitin sulfate ABC lyase I at 1.9 Å resolution. J Mol Biol. 328:623-634.
22. Huang W, Matte A, Li Y, Kim YS, Linhardt RJ, Su H, Cygler M. 1999. Crystal structure of chondroitinase B from Flavobacterium heparinum and its complex with a disaccharide product at 1.7 Å resolution. J Mol Biol. 294:1257-1269.
23. Lamzin VS, Dauter Z, Wilson KS. 1994. Dehydrogenation through the looking-glass. Nat Struct Biol. 1:281-282.
24. Lamzin VS, Dauter Z, Wilson KS. 1995. How nature deals with stereoisomers. Curr Opin Struct Biol. 5:830-836.
25. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Crystallogr. 26:283-291.
26. Li S, Kelly SJ, Lamani E, Ferraroni M, Jedrzejas MJ. 2000. Structural basis of hyaluronan degradation by Streptococcus pneumoniae hyaluronate lyase. EMBO J. 19:1228-1240.
27. Linn S, Chan T, Lipeski L, Salyers AA. 1983. Isolation and characterization of two chondroitin lyases from Bacteroides thetaiotaomicron. J Bacteriol. 156:859-866.
28. Lunin VV, Li Y, Linhardt RJ, Miyazono H, Kyogashima M, Kaneko T, Bell AW, Cygler M. 2004. High resolution crystal structure of Arthrobacter aurescens chondroitin AC lyase: Enzyme-substrate complex defines the catalytic mechanism. J Mol Biol. 337:367-386.
29. Mattevi A, Vanoni MA, Todone F, Rizzi M, Teplyakov A, Coda A, Bolognesi M, Curti B. 1996. Crystal structure of D-amino acid oxidase: A case of active site mirror-image convergent evolution with flavocytochrome b2. Proc Natl Acad Sci USA. 93:7496-7501.
30. Michel G, Pojasek K, Li Y, Sulea T, Linhardt RJ, Raman R, Prabhakar V, Sasisekharan R, Cygler M. 2004. The structure of chondroitin B lyase complexed with glycosaminoglycan oligosaccharides unravels a calcium-dependent catalytic machinery. J Biol Chem. 279:32882-32896.
31. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53:240-255.
32. Najmudin S, Andersen JT, Patkar SA, Borchert TV, Crout DH, Fulop V. 2003. Purification, crystallization and preliminary X-ray crystallographic studies on acetolactate decarboxylase. Acta Crystallogr, Sect D: Biol Crystallogr. 59:1073-1075.
33. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
34. Pawelek PD, Cheah J, Coulombe R, Macheroux P, Ghisla S, Vrielink A. 2000. The structure of L-amino acid oxidase reveals the substrate trajectory into an enantiomerically conserved active site. EMBO J. 19:4204-4215.
35. Pojasek K, Shriver Z, Kiley P, Venkataraman G, Sasisekharan R. 2001. Recombinant expression, purification, and kinetic characterization of chondroitinase AC and chondroitinase B from Flavobacterium heparinum Biochem Biophys Res Commun. 286:343-351.
36. Prabhakar V, Capila I, Bosques CJ, Pojasek K, Sashsekharan R. 2005. Chondroitinase ABC I from Proteus vulgaris: Cloning, recombinant expression and active site identification. Biochem J. 386:103-112.
37. Rye CS, Matte A, Cygler M, Withers SG. 2006. An atypical approach identifies TYR234 as the key base catalyst in chondroitin AC lyase. Chem biochem. 7:631-637.
38. Sambrook J, Russell D. 2001. Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
39. Shaya D, Tocilj A, Li Y, Myette J, Venkataraman G, Sasisekharan R, Cygler M. 2006. Crystal structure of heparinase II from Pedobacter heparinus and its complex with a disaccharide product. J Biol Chem. 281:15525-15535.
40. Sheldrick GM. 1991. Heavy atom location using SHELX-90. In: Wolf W, Evans PR, Leslie AG, editors. Isomorphous Replacement and Anomalous Scattering. Warrington: SERC Daresbury Laboratory. pp 80-86.
41. Tanner ME. 2002. Understanding nature's strategies for enzyme-catalyzed racemization and epimerization. Acc Chem Res. 35:237-246.
42. Terwilliger TC. 2002. Automated structure solution, density modification and model building. Acta Crystallogr, Sect D: Biol Crystallogr. 58:1937-1940.
43. Varki A. 1993. Biological roles of oligosaccharides: All of the theories are correct. Glycobiology. 3:97-130.
44. Vlodavsky I, Fuks Z, Ishai-Michaeli R, Bashkin P, Levi E, Korner G, Bar-Shavit R, Klagsbrun M. 1991. Extracellular matrix-resident basic fibroblast growth factor: Implication for the control of angiogenesis. J Cell Biochem. 45:167-176.
45. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, Hooper LV, Gordon JI. 2003. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science. 299:2074-2076.
46. Yoon HJ, Mikami B, Hashimoto W, Murata K. 1999. Crystal structure of alginate lyase A1-III from Sphingomonas species A1 at 1.78 Å resolution. J Mol Biol. 290:505-514.