Characterization of a multifunctional α2,3-sialyltransferase from Pasteurella dagmatis

Glycobiology

Volumn 23, Issue 11, 2013, Pages 1293-1304

  Schmölzer, Katharina ^a   Ribitsch, Doris ^a   Czabany, Tibor ^b   Luley Goedl, Christiane ^a   Kokot, Deja ^b   Lyskowski, Andrzej ^a   Zitzenbacher, Sabine ^a   Schwab, Helmut ^a,b   Nidetzky, Bernd ^a,b  

^a AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Bacterial sialyltransferase; Glycosyltransferase family Gt 80; N terminal elongation; Natural mutation; Structure function relationships

Indexed keywords

ALPHA 2,3 SIALIDASE; ALPHA 2,3 SIALYLTRANSFERASE; BACTERIAL ENZYME; BETA GALACTOSIDE; CYTIDINE 5' MONOPHOSPHATE N ACETYL NEURAMINIC HYDROLASE; GALACTOSE; HYDROLASE; SERINE; SIALIDASE; SIALYLTRANSFERASE; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; MICHAELIS CONSTANT; MUTATION; NONHUMAN; PASTEURELLA; PASTEURELLA DAGMATIS; PASTEURELLA MULTOCIDA; PH; PRIORITY JOURNAL; SIALYLATION;

BACTERIAL SIALYLTRANSFERASE; GLYCOSYLTRANSFERASE FAMILY GT-80; N-TERMINAL ELONGATION; NATURAL MUTATION; STRUCTURE-FUNCTION RELATIONSHIPS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CATALYTIC DOMAIN; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MONOSACCHARIDES; MUTAGENESIS, SITE-DIRECTED; PASTEURELLA; SIALIC ACIDS; SIALYLTRANSFERASES; SUBSTRATE SPECIFICITY;

EID: 84886051351     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt066     Document Type: Article

References (51)

1. Blixt O, Allin K, Pereira L, Datta A, Paulson JC. 2002. Efficient chemoenzymatic synthesis of O-linked sialyl oligosaccharides. J Am Chem Soc. 124:5739-5746. (Pubitemid 34533513)
2. Bojarova P, Rosencrantz RR, Elling L, Kren V. 2013. Enzymatic glycosylation of multivalent scaffolds. Chem Soc Rev. 42:4774-4797.
3. Cheng J, Huang S, Yu H, Li Y, Lau K, Chen X. 2010. Trans-sialidase activity of Photobacterium damselae α2,6-sialyltransferase and its application in the synthesis of sialosides. Glycobiology. 20:260-268.
4. Cheng J, Yu H, Lau K, Huang S, Chokhawala H, Li Y, Kumar V, Chen X. 2008. Multifunctionality of Campylobacter jejuni sialyltransferase CstII: Characterization of GD3/GT3 oligosaccharide synthase, GD3 oligosaccharide sialidase, and trans-sialidase activities. Glycobiology. 18:686-697.
5. Chiu CP, Watts AG, Lairson LL, Gilbert M, Lim D, Wakarchuk WW, Withers SG, Strynadka NCJ. 2004. Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog. Nature Struct Mol Biol. 11:163-170. (Pubitemid 38146520)
6. Coutinho PM, Deleury E, Davies GJ, Henrissat B. 2003. An evolving hierarchical family classification for glycosyltransferases. J Mol Biol. 328:307-317. (Pubitemid 36407576)
7. Damager I, Buchini S, Amaya MF, Buschiazzo A, Alzari P, Frasch AC, Watts A, Withers SG. 2008. Kinetic and mechanistic analysis of Trypanosoma cruzi trans-sialidase reveals a classical Ping-Pong mechanism with acid/base catalysis. Biochemistry. 47:3507-3512. (Pubitemid 351399239)
8. Fersht A. 1998. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding. 1st ed. New York: Freeman, W.H. & Company.
9. Gilbert M, Watson DC, Cunningham AM, Jennings MP, Young NM,Wakarchuk WW. 1996. Cloning of the lipooligosaccharide α2,3-sialyltransferase from the bacterial pathogens Neisseria meningitidis and Neisseria gonorrhoeae. J Biol Chem. 271:28271-28276. (Pubitemid 26374640)
10. Iwatani T, Okino N, Sakakura M, Kajiwara H, Takakura Y, Kimura M, Ito M, Yamamoto T, Kakuta Y. 2009. Crystal structure of α/β-galactoside α-2,3-sialyltransferase from a luminous marine bacterium, Photobacterium phosphoreum. FEBS Lett. 583:2083-2087.
11. Kajiwara H, Katayama S, Kakuta Y, Okino N, Ito M, Mine T, Yamamoto T.2012. Loss-of-function mutation in bi-functional marine bacterial sialyltransferase. Biosci Biotechnol Biochem. 76:1639-1644.
12. Kakuta Y, Okino N, Kajiwara H, Ichikawa M, Takakura Y, Ito M, Yamamoto T. 2008. Crystal structure of Vibrionaceae Photobacterium sp. JT-ISH-224 α-2,6-sialyltransferase in a ternary complex with donor product CMP and acceptor substrate lactose: Catalytic mechanism and substrate recognition. Glycobiology. 18:66-73.
13. Kondadi PK, Rossi M, Twelkmeyer B, Schur MJ, Li J, Schott T, Paulin L, Auvinen P, Hänninen ML, Schweda EKH, et al. 2012. Identification and characterization of a lipopolysaccharide α2,3-sialyltransferase from the human pathogen Helicobacter bizzozeronii. J Bacteriol. 194:2540-2550.
14. Krieger E, Darden T, Nabuurs SB, Finkelstein A, Vriend G. 2004. Making optimal use of empirical energy functions: Force-field parameterization in crystal space. Proteins. 57:678-683. (Pubitemid 39626989)
15. Krieger E, Koraimann G, Vriend G. 2002. Increasing the precision of comparative models with YASARA NOVA-a self-parameterizing force field. Proteins. 47:393-402. (Pubitemid 34438688)
16. Lau K, Yu H, Thon V, Khedri Z, Leon ME, Tran BK, Chen X. 2011. Sequential two-step multienzyme synthesis of tumor-associated sialyl T-antigens and derivatives. Org Biomol Chem. 9:2784-2789.
17. Li Y, Chen X. 2012. Sialic acid metabolism and sialyltransferases: natural functions and applications. Appl Microbiol Biotechnol. 94:887-905.
18. Li Y, Sun M, Huang S, Yu H, Chokhawala HA, Thon V, Chen X. 2007. The Hd0053 gene of Haemophilus ducreyi encodes an α2,3-sialyltransferase. Biochem Biophys Res Commun. 361:555-560. (Pubitemid 47187287)
19. Lin LYC, Rakic B, Chiu CPC, Lameignere E, Wakarchuk WW, Withers SG, Strynadka NCJ. 2011. Structure and mechanism of the lipooligosaccharide sialyltransferase from Neisseria meningitidis. J Biol Chem. 286:37237-37248.
20. Malekan H, Fung G, Thon V, Khedri Z, Yu H, Qu J, Li Y, Ding L, Lam KS, Chen X. 2013. One-pot multi-enzyme (OPME) chemoenzymatic synthesis of sialyl-Tn-MUC1 and sialyl-T-MUC1 glycopeptides containing natural or non-natural sialic acid. Bioorg Med Chem. 21:4778-4785.
21. Milac AL, Buchete NV, Fritz TA, Hummer G, Tabak LA. 2007. Substrateinduced conformational changes and dynamics of UDP-N- acetylgalactosamine: polypeptide N-acetylgalactosaminyltransferase-2. JMol Biol. 373:439-451. (Pubitemid 47445582)
22. Mine T, Katayama S, Kajiwara H, Tsunashima M, Tsukamoto H, Takakura Y, Yamamoto T. 2010. An α2,6-sialyltransferase cloned from Photobacterium leiognathi strain JT-SHIZ-119 shows both sialyltransferase and neuraminidase activity. Glycobiology. 20:158-165.
23. Nagashima I, Mine T, Yamamoto T, Shimizu H. 2012. Efficiency of organic solvents on the ability of α2,3-sialyltransferase from Photobacterium sp. JT-ISH-224 to control a hydrolysis side reaction. Carbohydr Res. 358:31-36.
24. Newman J. 2004. Novel buffer systems for macromolecular crystallization. Acta Crystallogr Sect D. 60:610-612. (Pubitemid 41087612)
25. Ni L, Chokhawala HA, Cao H, Henning R, Ng L, Huang S, Yu H, Chen X, Fisher AJ. 2007. Crystal structures of Pasteurella multocida sialyltransferase complexes with acceptor and donor analogues reveal substrate binding sites and catalytic mechanism. Biochemistry. 46:6288-6298. (Pubitemid 46842872)
26. Ni L, Sun M, Yu H, Chokhawala H, Chen X, Fisher AJ. 2006. Cytidine 5′-monophosphate (CMP)-induced structural changes in a multifunctional sialyltransferase from Pasteurella multocida. Biochemistry. 45:2139-2148. (Pubitemid 43271314)
27. Oh TJ, Kim DH, Kang SY, Yamaguchi T, Sohng JK. 2011. Enzymatic synthesis of vancomycin derivatives using galactosyltransferase and sialyltransferase. J Antibiot. 64:103-109.
28. Palcic MM. 2011. Glycosyltransferases as biocatalysts. Curr Opin Chem Biol. 15:226-233.
29. Qasba PK, Ramakrishnan B, Boeggeman E. 2005. Substrate-induced conformational changes in glycosyltransferases. Trends in Biochemical Sciences. 30:53-62. (Pubitemid 40093741)
30. Schauer R. 2009. Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol. 19:507-514.
31. Schenkman S, Jiang MS, Hart GW, Nussenzweig V. 1991. A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell. 65:1117-1125. (Pubitemid 121001326)
32. Schur MJ, Lameignere E, Strynadka NC, Wakarchuk WW. 2012. Characterization of α2,3- and α2,6-sialyltransferases from Helicobacter acinonychis. Glycobiology. 22:997-1006.
33. Scudder PR, Chantler EN. 1981. Glycosyltransferases of the human cervical epithelium II. Characterization of a CMP-N-acetylneuraminate: Galactosylglycoprotein sialyltransferase. Biochim Biophys Acta Enzymol. 660:136-141. (Pubitemid 11045618)
34. Shaikh FA, Withers SG. 2008. Teaching old enzymes new tricks: engineering and evolution of glycosidases and glycosyl transferases for improved glycoside synthesis. Biochem Cell Biol. 86:169-177. (Pubitemid 351536497)
35. Sugiarto G, Lau K, Li Y, Khedri Z, Yu H, Le DT, Chen X. 2011. Decreasing the sialidase activity of multifunctional Pasteurella multocida α2- 3-sialyltransferase 1 (PmST1) by site-directed mutagenesis. Mol Bio Syst. 7:3021-3027.
36. x. ACS Chem Biol. 7:1232-1240.
37. Sun M, Li Y, Chokhawala HA, Henning R, Chen X. 2008. N-Terminal 112 amino acid residues are not required for the sialyltransferase activity of Photobacterium damselae α-2,6-sialyltransferase. Biotechnol Lett. 30:671-676.
38. Takakura Y, Tsukamoto H, Yamamoto T. 2007. Molecular cloning, expression and properties of an α/β-galactoside α2,3-sialyltransferase from Vibrio sp. JT-FAJ-16. J Biochem. 142:403-412. (Pubitemid 350221844)
39. Thon V, Lau K, Yu H, Tran BK, Chen X. 2011. PmST2: A novel Pasteurella multocida glycolipid α2,3-sialyltransferase. Glycobiology. 21:1206-1216.
40. Tsukamoto H, Takakura Y, Mine T, Yamamoto T. 2008. Photobacterium sp. JT-ISH-224 produces two sialyltransferases, α/β-galactoside α2,3-sialyltransferase and β-galactoside α2,6- sialyltransferase. J Biochem. 143: 187-197. (Pubitemid 351238161)
41. Tsukamoto H, Takakura Y, Yamamoto T. 2007. Purification, cloning, and expression of an α/β-galactoside α-2,3-sialyltransferase from a luminous marine bacterium, Photobacterium phosphoreum. J Biol Chem. 282:29794-29802. (Pubitemid 350041548)
42. Varki A. 2008. Sialic acids in human health and disease. Trends Mol Med. 14:351-360.
43. Watson DC, Leclerc S,Wakarchuk WW, Young NM. 2011. Enzymatic synthesis and properties of glycoconjugates with legionaminic acid as replacement for neuraminic acid. Glycobiology. 21:99-108.
44. Yamamoto T, Hamada Y, Ichikawa M, Kajiwara H, Mine T, Tsukamoto H, Takakura Y. 2007. A β-galactoside α2,6-sialyltransferase produced by a marine bacterium, Photobacterium leiognathi JT-SHIZ-145, is active at pH 8. Glycobiology. 17:1167-1174. (Pubitemid 47604724)
45. Yamamoto T, Ichikawa M, Takakura Y. 2008. Conserved amino acid sequences in the bacterial sialyltransferases belonging to glycosyltransferase family 80. Biochem Biophys Res Commun. 365:340-343. (Pubitemid 350137294)
46. Yamamoto T, Nakashizuka M, Kodama H, Kajihara Y, Terada I. 1996. Purification and characterization of a marine bacterial β-galactoside α2,6-sialyltransferase from Photobacterium damselae JT0160. J Biochem. 120:104-110. (Pubitemid 26258255)
47. Yamamoto T, Takakura Y, Tsukamoto H. 2006. Bacterial sialyltransferases. Trends Glycosci Glycotechnol. 18:253-265. (Pubitemid 44475086)
48. Yu H, Chokhawala HA, Huang S, Chen X. 2006. One-pot three-enzyme chemoenzymatic approach to the synthesis of sialosides containing natural and non-natural functionalities. Nat Protocols. 1:2485-2492.
49. Yu H, Chokhawala H, Karpel R, Yu H, Wu B, Zhang J, Zhang Y, Jia Q, Chen X. 2005. A multifunctional Pasteurella multocida sialyltransferase: A powerful tool for the synthesis of sialoside libraries. J Am Chem Soc. 127:17618-17619. (Pubitemid 43003372)
50. Yu H, Huang S, Chokhawala H, Sun M, Zheng H, Chen X. 2006. Highly efficient chemoenzymatic synthesis of naturally occurring and nonnatural α-2,6-linked sialosides: A P. damselae α-2,6-sialyltransferase with extremely flexible donor-substrate specificity. Angew Chem Int Ed. 45:3938-3944. (Pubitemid 44105691)
51. Zhuo Y, Bellis SL. 2011. Emerging role of α2,6-sialic acid as a negative regulator of galectin binding and function. J Biol Chem. 286:5935-5941.