Crystal structures of sialyltransferase from Photobacterium damselae

FEBS Letters

Volumn 588, Issue 24, 2014, Pages 4720-4729

  Huynh, Nhung ^a,b   Li, Yanhong ^a   Yu, Hai ^a   Huang, Shengshu ^a   Lau, Kam ^a,c   Chen, Xi ^a   Fisher, Andrew J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c GRIFFITH UNIVERSITY   (Australia)

Author keywords

CMP 3F(a)Neu5Ac; Photobacterium damselae; Protein crystal structure; Sialic acid; 2 6 Sialyltransferase

Indexed keywords

CYTIDINE 5' MONOPHOSPHATE 3 FLUORO(AXIAL) N ACETYLNEURAMINIC ACID; IMMUNOGLOBULIN; N ACETYLNEURAMINIC ACID; SIALYLTRANSFERASE; UNCLASSIFIED DRUG; BETA-D-GALACTOSIDE ALPHA 2-6-SIALYLTRANSFERASE; CYTIDINE PHOSPHATE N ACETYLNEURAMINIC ACID; METAL;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; METAL BINDING; MICHAELIS CONSTANT; NONHUMAN; PHOTOBACTERIUM DAMSELAE; PROTEIN DOMAIN; PROTEIN FOLDING; STRUCTURE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; METABOLISM; PHOTOBACTERIUM; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

PHOTOBACTERIUM DAMSELAE;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYTIDINE MONOPHOSPHATE N-ACETYLNEURAMINIC ACID; METALS; MODELS, MOLECULAR; PHOTOBACTERIUM; PROTEIN STRUCTURE, TERTIARY; SIALYLTRANSFERASES;

EID: 84915745108     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.11.003     Document Type: Article

References (50)

1. X. Chen, and A. Varki Advances in the biology and chemistry of sialic acids ACS Chem. Biol. 5 2010 163 176
2. L. Ni, M. Sun, H. Yu, H. Chokhawala, X. Chen, and A.J. Fisher Cytidine 5′-monophosphate (CMP)-induced structural changes in a multifunctional sialyltransferase from Pasteurella multocida Biochemistry 45 2006 2139 2148
3. R. Schauer Chemistry, metabolism, and biological functions of sialic acids Adv. Carbohydr. Chem. Biochem. 40 1982 131 234
4. C.D. Rillahan, A. Antonopoulos, C.T. Lefort, R. Sonon, P. Azadi, K. Ley, A. Dell, S.M. Haslam, and J.C. Paulson Global metabolic inhibitors of sialyl- and fucosyltransferases remodel the glycome Nat. Chem. Biol. 8 2012 661 668
5. A. Harduin-Lepers, M.A. Recchi, and P. Delannoy 1994, the year of sialyltransferases Glycobiology 5 1995 741 758
6. H. Yu, H. Chokhawala, R. Karpel, H. Yu, B. Wu, J. Zhang, Y. Zhang, Q. Jia, and X. Chen A multifunctional Pasteurella multocida sialyltransferase: a powerful tool for the synthesis of sialoside libraries J. Am. Chem. Soc. 127 2005 17618 17619
7. J. Cheng, H. Yu, K. Lau, S. Huang, H.A. Chokhawala, Y. Li, V.K. Tiwari, and X. Chen Multifunctionality of Campylobacter jejuni sialyltransferase CstII: characterization of GD3/GT3 oligosaccharide synthase, GD3 oligosaccharide sialidase, and trans-sialidase activities Glycobiology 18 2008 686 697
8. J. Cheng, S. Huang, H. Yu, Y. Li, K. Lau, and X. Chen Trans-sialidase activity of Photobacterium damsela α2,6-sialyltransferase and its application in the synthesis of sialosides Glycobiology 20 2010 260 268
9. J.A. Campbell, G.J. Davies, V. Bulone, and B. Henrissat A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities Biochem. J. 326 Pt 3 1997 929 939
10. P. Coutinho, E. Deleury, G. Davies, and B. Henrissat An evolving hierarchical family classification for glycosyltransferases J. Mol. Biol. 328 2003 307 317
11. F.V. Rao, J.R. Rich, B. Rakic, S. Buddai, M.F. Schwartz, K. Johnson, C. Bowe, W.W. Wakarchuk, S. Defrees, S.G. Withers, and N.C. Strynadka Structural insight into mammalian sialyltransferases Nat. Struct. Mol. Biol. 16 2009 1186 1188
12. L. Meng, F. Forouhar, D. Thieker, Z. Gao, A. Ramiah, H. Moniz, Y. Xiang, J. Seetharaman, S. Milaninia, M. Su, R. Bridger, L. Veillon, P. Azadi, G. Kornhaber, L. Wells, G.T. Montelione, R.J. Woods, L. Tong, and K.W. Moremen Enzymatic basis for N-glycan sialylation: structure of rat alpha2,6-sialyltransferase (ST6GAL1) reveals conserved and unique features for glycan sialylation J. Biol. Chem. 288 2013 34680 34698
13. C.P. Chiu, A.G. Watts, L.L. Lairson, M. Gilbert, D. Lim, W.W. Wakarchuk, S.G. Withers, and N.C. Strynadka Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog Nat. Struct. Mol. Biol. 11 2004 163 170
14. C.P. Chiu, L.L. Lairson, M. Gilbert, W.W. Wakarchuk, S.G. Withers, and N.C. Strynadka Structural analysis of the alpha-2,3-sialyltransferase Cst-I from Campylobacter jejuni in apo and substrate-analogue bound forms Biochemistry 46 2007 7196 7204
15. L.Y. Lin, B. Rakic, C.P. Chiu, E. Lameignere, W.W. Wakarchuk, S.G. Withers, and N.C. Strynadka Structure and mechanism of the lipooligosaccharide sialyltransferase from Neisseria meningitidis J. Biol. Chem. 286 2011 37237 37248
16. L. Ni, H.A. Chokhawala, H. Cao, R. Henning, L. Ng, S. Huang, H. Yu, X. Chen, and A.J. Fisher Crystal structures of Pasteurella multocida sialyltransferase complexes with acceptor and donor analogues reveal substrate binding sites and catalytic mechanism Biochemistry 46 2007 6288 6298
17. D.U. Kim, J.H. Yoo, Y.J. Lee, K.S. Kim, and H.S. Cho Structural analysis of sialyltransferase PM0188 from Pasteurella multocida complexed with donor analogue and acceptor sugar BMB Rep. 41 2008 48 54
18. Y. Kakuta, N. Okino, H. Kajiwara, M. Ichikawa, Y. Takakura, M. Ito, and T. Yamamoto Crystal structure of Vibrionaceae Photobacterium sp. JT-ISH-224 α2,6-sialyltransferase in a ternary complex with donor product CMP and acceptor substrate lactose: catalytic mechanism and substrate recognition Glycobiology 18 2008 66 73
19. T. Iwatani, N. Okino, M. Sakakura, H. Kajiwara, Y. Takakura, M. Kimura, M. Ito, T. Yamamoto, and Y. Kakuta Crystal structure of alpha/beta-galactoside alpha2,3-sialyltransferase from a luminous marine bacterium Photobacterium phosphoreum FEBS Lett. 583 2009 2083 2087
20. Y. Li, and X. Chen Sialic acid metabolism and sialyltransferases: natural functions and applications Appl. Microbiol. Biotechnol. 94 2012 887 905
21. C. Breton, L. Snajdrova, C. Jeanneau, J. Koca, and A. Imberty Structures and mechanisms of glycosyltransferases Glycobiology 16 2006 29R 37R
22. M. Audry, C. Jeanneau, A. Imberty, A. Harduin-Lepers, P. Delannoy, and C. Breton Current trends in the structure-activity relationships of sialyltransferases Glycobiology 21 2011 716 726
23. M. Sun, Y. Li, H.A. Chokhawala, R. Henning, and X. Chen N-Terminal 112 amino acid residues are not required for the sialyltransferase activity of Photobacterium damsela alpha2,6-sialyltransferase Biotechnol. Lett. 30 2008 671 676
24. H. Yu, S. Huang, H. Chokhawala, M. Sun, H. Zheng, and X. Chen Highly efficient chemoenzymatic synthesis of naturally occurring and non-natural alpha-2,6-linked sialosides: a P. damsela alpha-2,6-sialyltransferase with extremely flexible donor-substrate specificity Angew. Chem. Int. Ed. Engl. 45 2006 3938 3944
25. T. Yamamoto, M. Nakashizuka, and I. Terada Cloning and expression of a marine bacterial beta-galactoside alpha2,6-sialyltransferase gene from Photobacterium damsela JT0160 J. Biochem. 123 1998 94 100
26. G. Sugiarto, K. Lau, Y. Li, Z. Khedri, H. Yu, D.T. Le, and X. Chen Decreasing the sialidase activity of multifunctional Pasteurella multocida alpha2-3-sialyltransferase 1 (PmST1) by site-directed mutagenesis Mol. BioSyst. 7 2011 3021 3027
27. G. Sugiarto, K. Lau, J. Qu, Y. Li, S. Lim, S. Mu, J.B. Ames, A.J. Fisher, and X. Chen A sialyltransferase mutant with decreased donor hydrolysis and reduced sialidase activities for directly sialylating Lewis(x) ACS Chem. Biol. 7 2012 1232 1240
28. H.A. Chokhawala, H. Cao, H. Yu, and X. Chen Enzymatic synthesis of fluorinated mechanistic probes for sialidases and sialyltransferases J. Am. Chem. Soc. 129 2007 10630 10631
29. T.G. Battye, L. Kontogiannis, O. Johnson, H.R. Powell, and A.G. Leslie IMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM Acta Crystallogr. D Biol. Crystallogr. 67 2011 271 281
30. P. Evans Scaling and assessment of data quality Acta Crystallogr. D Biol. Crystallogr. 62 2006 72 82
31. A.J. McCoy, R.W. Grosse-Kunstleve, L.C. Storoni, and R.J. Read Likelihood-enhanced fast translation functions Acta Crystallogr. D Biol. Crystallogr. 61 2005 458 464
32. P.D. Adams, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, N.W. Moriarty, R.J. Read, J.C. Sacchettini, N.K. Sauter, and T.C. Terwilliger PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr. D Biol. Crystallogr. 58 2002 1948 1954
33. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
34. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P.H. Zwart PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
35. V. Schomaker, and K.N. Trueblood On the rigid-body motion of molecules in crystals Acta Crystallogr. Sect. B 24 1968 63 76
36. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Cryst. 26 1993 283 291
37. M. Muda, N.N. Rao, and A. Torriani Role of PhoU in phosphate transport and alkaline phosphatase regulation J. Bacteriol. 174 1992 8057 8064
38. S. Jain, W.B. Drendel, Z.W. Chen, F.S. Mathews, W.S. Sly, and J.H. Grubb Structure of human beta-glucuronidase reveals candidate lysosomal targeting and active-site motifs Nat. Struct. Biol. 3 1996 375 381
39. A. Chang, S. Singh, G.N. Phillips Jr., and J.S. Thorson Glycosyltransferase structural biology and its role in the design of catalysts for glycosylation Curr. Opin. Biotechnol. 22 2011 800 808
40. U.M. Unligil, and J.M. Rini Glycosyltransferase structure and mechanism Curr. Opin. Struct. Biol. 10 2000 510 517
41. T. Mine, S. Katayama, H. Kajiwara, M. Tsunashima, H. Tsukamoto, Y. Takakura, and T. Yamamoto An α2,6-sialyltransferase cloned from Photobacterium leiognathi strain JT-SHIZ-119 shows both sialyltransferase and neuraminidase activity Glycobiology 20 2010 158 165
42. T. Yamamoto, Y. Hamada, M. Ichikawa, H. Kajiwara, T. Mine, H. Tsukamoto, and Y. Takakura A β-galactoside α2,6-sialyltransferase produced by a marine bacterium, Photobacterium leiognathi JT-SHIZ-145, is active at pH 8 Glycobiology 17 2007 1167 1174
43. J. Liu, Y. Lou, H. Yokota, P.D. Adams, R. Kim, and S.H. Kim Crystal structure of a PhoU protein homologue: a new class of metalloprotein containing multinuclear iron clusters J. Biol. Chem. 280 2005 15960 15966
44. N. Echols, N. Morshed, P.V. Afonine, A.J. McCoy, M.D. Miller, R.J. Read, J.S. Richardson, T.C. Terwilliger, and P.D. Adams Automated identification of elemental ions in macromolecular crystal structures Acta Crystallogr. D Biol. Crystallogr. 70 2014 1104 1114
45. H. Zheng, M.D. Chordia, D.R. Cooper, M. Chruszcz, P. Muller, G.M. Sheldrick, and W. Minor Validation of metal-binding sites in macromolecular structures with the CheckMyMetal web server Nat. Protoc. 9 2014 156 170
46. Y. Hu, L. Chen, S. Ha, B. Gross, B. Falcone, D. Walker, M. Mokhtarzadeh, and S. Walker Crystal structure of the MurG:UDP-GlcNAc complex reveals common structural principles of a superfamily of glycosyltransferases Proc. Natl. Acad. Sci. U.S.A. 100 2003 845 849
47. S. Morera, A. Imberty, U. Aschke-Sonnenborn, W. Ruger, and P. Freemont T4 phage beta-glucosyltransferase: substrate binding and proposed catalytic mechanism J. Mol. Biol. 292 1999 717 730
48. A.M. Mulichak, H.C. Losey, C.T. Walsh, and R.M. Garavito Structure of the UDP-glucosyltransferase GtfB that modifies the heptapeptide aglycone in the biosynthesis of vancomycin group antibiotics Structure 9 2001 547 557
49. K. Fox, A. Cox, M. Gilbert, W. Wakarchuk, J. Li, K. Makepeace, J. Richards, E. Moxon, and D. Hood Identification of a bifunctional lipopolysaccharide sialyltransferase in Haemophilus influenzae: incorporation of disialic acid J. Biol. Chem. 281 2006 40024 40032
50. F. Freiberger, H. Claus, A. Gunzel, I. Oltmann-Norden, J. Vionnet, M. Muhlenhoff, U. Vogel, W.F. Vann, R. Gerardy-Schahn, and K. Stummeyer Biochemical characterization of a Neisseria meningitidis polysialyltransferase reveals novel functional motifs in bacterial sialyltransferases Mol. Microbiol. 65 2007 1258 1275