Structural and biochemical characterization of the broad substrate specificity of Bacteroides thetaiotaomicron commensal sialidase

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 8, 2013, Pages 1510-1519

  Park, Kwang Hyun ^a,b   Kim, Min Gyu ^c   Ahn, Hee Jeong ^c   Lee, Dae Han ^c   Kim, Jin Hyo ^d   Kim, Young Wan ^c   Woo, Eui Jeon ^a,b  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b University of Science and Technology (UST)   (South Korea)

^c Korea University   (South Korea)

^d National Institute of Animal Science   (South Korea)

Author keywords

Bacteroides thetaiotaomicron; Carbohydrate binding domain; Protein structure; Sialidase; Substrate specificity

Indexed keywords

N ACETYLNEURAMINIC ACID; SIALIDASE; 2-DEOXY-2,3-DEHYDRO-N-ACETYLNEURAMINIC ACID; DRUG DERIVATIVE; N ACETYL 2,3 DIDEHYDRO 2 DEOXYNEURAMINIC ACID; RECOMBINANT PROTEIN; SULFONIC ACID DERIVATIVE;

ARTICLE; BACTEROIDES THETAIOTAOMICRON; COMMENSAL; ENZYME ACTIVITY; ENZYME SPECIFICITY; HYDROLYSIS KINETICS; INHIBITION KINETICS; MOLECULAR MODEL; NONHUMAN; PARAMETERS; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; BACTEROIDES; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETICS; HUMAN; HYDROLYSIS; KINETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

BACTEROIDES THETAIOTAOMICRON;

AMINO ACID SEQUENCE; BACTEROIDES; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HUMANS; HYDROLYSIS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; SULFONIC ACIDS;

EID: 84882267201     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.04.028     Document Type: Article

References (45)

1. R. Schauer, Chemistry, metabolism, and biological functions of sialic acids, Adv. Carbohydr. Chem. Biochem. 40 (1982) 131-234.
2. S. Kelm, R. Schauer, Sialic acids in molecular and cellular interactions, Int. Rev. Cytol. 175 (1997) 137-240. (Pubitemid 27309809)
3. S.L Newstead, JA Potter, J.C Wilson, G. Xu, C.H. Chien, A.G. Watts, S.G. Withers, G.L Taylor, The structure of Clostridium perfringens NanI sialidase and its catalytic intermediates, J. Biol. Chem. 283 (2008) 9080-9088.
4. S. Crennell, T. Takimoto, A. Portner, G. Taylor, Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase, Nat. Struct. Biol. 7 (2000) 1068-1074.
5. J.N. Varghese, W.G. Laver, P.M. Colman, Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 A resolution, Nature 303 (1983) 35-40. (Pubitemid 13125070)
6. S.J. Crennell, E.F. Garman, W.G. Laver, E.R. Vimr, G.L. Taylor, Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase, Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 9852-9856. (Pubitemid 23328208)
7. S. Crennell, E. Garman, G. Laver, E. Vimr, G. Taylor, Crystal structure of Vibrio cholerae neuraminidase reveals dual lectin-like domains in addition to the catalytic domain, Structure 2 (1994) 535-544.
8. R.M. Domingues, S.M. Cavalcanti, A.F. Andrade, M.C. Ferreira, Sialic acidas receptor of Bacteroides fragilis lectin-like adhesin, Zentralbl. Bakteriol. 277 (1992) 340-344.
9. C.A. Guzman, M. Plate, C. Pruzzo, Role of neuraminidase-dependent adherence in Bacteroides fragilis attachment to human epithelial cells, FEMS Microbiol. Lett. 59 (1990) 187-192. (Pubitemid 20256296)
10. V. Rogemond, R.M. Guinet, Lectinlike adhesins in the Bacteroides fragilis group, Infect. Immun. 53 (1986) 99-102. (Pubitemid 16084370)
11. E. Feng, W.J. Shin, X. Zhu, J. Li, D. Ye, J. Wang, M. Zheng, J.P. Zuo, K.T. No, X. Liu, W. Zhu, W. Tang, B.L. Seong, H. Jiang, H. Liu, Structure-based design and synthesis of C-1- and C-4-modified analogs of zanamivir as neuraminidase inhibitors, J. Med. Chem. 56 (2013) 671-684.
12. Y. Shan, Y. Ma, M. Wang, Y. Dong, Recent advances in the structure-based design of neuraminidase inhibitors as antiinfluenza agents, Curr. Med. Chem. 19 (2012) 5885-5894.
13. A.A. Salyers, Bacteroides of the human lower intestinal tract, Annu. Rev. Microbiol. 38 (1984) 293-313.
14. P.B. Eckburg, E.M. Bik, C.N. Bernstein, E. Purdom, L. Dethlefsen, M. Sargent, S.R. Gill, K.E. Nelson, D.A. Relman, Diversity of the human intestinal microbial flora, Science 308 (2005) 1635-1638. (Pubitemid 40807514)
15. J. Xu, H.C. Chiang, M.K. Bjursell, J.I. Gordon, Message from a human gut symbiont: sensitivity is a prerequisite for sharing, Trends Microbiol. 12 (2004) 21-28. (Pubitemid 38045256)
16. J. Xu, M.K. Bjursell, J. Himrod, S. Deng, L.K. Carmichael, H.C. Chiang, L.V. Hooper, J.I. Gordon, A genomic view of the human-Bacteroides thetaiotaomicron symbiosis, Science 299 (2003) 2074-2076. (Pubitemid 36383735)
17. J. Xu, J.I. Gordon, Honor thy symbionts, Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 10452-10459. (Pubitemid 37071899)
18. A.R. Reeves, J.N. D'Elia, J. Frias, A.A. Salyers, A Bacteroides thetaiotaomicron outer membrane protein that is essential for utilization of maltooligosaccharides and starch, J. Bacteriol. 178 (1996) 823-830. (Pubitemid 26036656)
19. L.V. Hooper, T. Midtvedt, J.I. Gordon, How host-microbial interactions shape the nutrient environment of the mammalian intestine, Annu. Rev. Nutr. 22 (2002) 283-307. (Pubitemid 35221463)
20. S.R. Gill, M. Pop, R.T. Deboy, P.B. Eckburg, P.J. Turnbaugh, B.S. Samuel, J.I. Gordon, D.A. Relman, C.M. Fraser-Liggett, K.E. Nelson, Metagenomic analysis of the human distal gut microbiome, Science 312 (2006) 1355-1359. (Pubitemid 43839542)
21. R.E. Ley, F. Backhed, P. Turnbaugh, C.A. Lozupone, R.D. Knight, J.I. Gordon, Obesity alters gut microbial ecology, Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 11070-11075. (Pubitemid 41105994)
22. R.E. Ley, P.J. Turnbaugh, S. Klein, J.I. Gordon, Microbial ecology: human gut microbes associated with obesity, Nature 444 (2006) 1022-1023. (Pubitemid 46018512)
23. J. Sambrook, E.F. Fritsch, T. Maniatis, Molecular cloning: a laboratory manual, Cold Spring Harbor Laboratory Press, New York, 1989.
24. M. Chandler, M.J. Bamford, R. Conroy, B. Lamont, V.K. Patel, I.P. Steeples, R. Storer, N.G. Weir, M. Wright, C. Williamson, Synthesis of the potent influenza neuramini-dase inhibitor 4-guanidino Neu5Ac2en. X-Ray molecular structure of 5-acetamido-4-amino-2,6-anhydro-3,4,5-trideoxy-D-erythro-L-gluco- nononic acid, J. Chem. Soc., Perkin Trans. 1 (9) (1995) 1173-1180.
25. K. Sugahara, K. Sugimoto, O. Nomura, T. Usui, Enzymatic assay of serum sialic acid, Clin. Chim. Acta 108 (1980) 493-498. (Pubitemid 11192723)
26. T.N. Petersen, S. Brunak, G. von Heijne, H. Nielsen, SignalP 4.0: discriminating signal peptides from transmembrane regions, Nat. Methods 8 (2011) 785-786.
27. P. Roggentin, R. Schauer, L.L. Hoyer, E.R. Vimr, The sialidase superfamily and its spread by horizontal gene transfer, Mol. Microbiol. 9 (1993) 915-921. (Pubitemid 23271769)
28. P. Hunt, The biological significance and therapeutic potential of megakaryocyte growth and development factor (Mpl-ligand), Transfus. Sci. 17 (1996) 347-348. (Pubitemid 26326785)
29. F.G. Hayden, B.S. Rollins, L.K. Madren, Anti-influenza virus activity of the neuraminidase inhibitor 4-guanidino-Neu5Ac2en in cell culture and in human respiratory epithelium, Antiviral Res. 25 (1994) 123-131. (Pubitemid 24308529)
30. M.F. Amaya, A. Buschiazzo, T. Nguyen, P.M. Alzari, The high resolution structures of free and inhibitor-bound Trypanosoma rangeli sialidase and its comparison with T. cruzi trans-sialidase, J. Mol. Biol. 325 (2003) 773-784. (Pubitemid 36268697)
31. A. Buschiazzo, P.M. Alzari, Structural insights into sialic acid enzymology, Curr. Opin. Chem. Biol. 12 (2008) 565-572.
32. W.P. Burmeister, B. Henrissat, C. Bosso, S. Cusack, R.W. Ruigrok, Influenza B virus neuraminidase can synthesize its own inhibitor, Structure 1 (1993) 19-26.
33. S.J. Crennell, E.F. Garman, C. Philippon, A. Vasella, W.G. Laver, E.R. Vimr, G.L. Taylor, The structures of Salmonella typhimurium LT2 neuraminidase and its complexes with three inhibitors at high resolution, J. Mol. Biol. 259 (1996) 264-280. (Pubitemid 26178118)
34. K.E. Achyuthan, A.M. Achyuthan, Comparative enzymology, biochemistry and pathophysiology of human exo-alpha-sialidases (neuraminidases), Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129 (2001) 29-64. (Pubitemid 32401124)
35. G. Xu, J.A. Potter, R.J. Russell, M.R. Oggioni, P.W. Andrew, G.L. Taylor, Crystal structure of the NanB sialidase from Streptococcus pneumoniae, J. Mol. Biol. 384 (2008) 436-449.
36. A.B. Boraston, E. Ficko-Blean, M. Healey, Carbohydrate recognition by a large sialidase toxin from Clostridium perfringens, Biochemistry 46 (2007) 11352-11360. (Pubitemid 47556762)
37. L.E. Comstock, M.J. Coyne, Bacteroides thetaiotaomicron: a dynamic, nicheadapted human symbiont, Bioessays 25 (2003) 926-929. (Pubitemid 37221516)
38. J.L. Sonnenburg, C.T. Chen, J.I. Gordon, Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host, PLoS Biol. 4 (2006) e413.
39. M.A. Zocco, M.E. Ainora, G. Gasbarrini, A. Gasbarrini, Bacteroides thetaiotaomicron in the gut: molecular aspects of their interaction, Dig. Liver Dis. 39 (2007) 707-712. (Pubitemid 47046634)
40. A. Varki, Diversity in the sialic acids, Glycobiology 2 (1992) 25-40.
41. M. Kiyohara, K. Tanigawa, T. Chaiwangsri, T. Katayama, H. Ashida, K. Yamamoto, An exo-alpha-sialidase from bifidobacteria involved in the degradation of sialyloligosaccharides in human milk and intestinal glycoconjugates, Glycobiology 21 (2011) 437-447.
42. S. Kim, D.B. Oh, O. Kwon, H.A. Kang, Identification and functional characterization of the NanH extracellular sialidase from Corynebacterium diphtheriae, J. Biochem. 147 (2010) 523-533.
43. S.L. Newstead, J.N. Watson, A.J. Bennet, G. Taylor, Galactose recognition by the carbohydrate-binding module of a bacterial sialidase, Acta Crystallogr. D Biol. Crystallogr. 61 (2005) 1483-1491. (Pubitemid 43934584)
44. H. Gut, S.J. King, M.A. Walsh, Structural and functional studies of Streptococcus pneumoniae neuraminidase B: an intramolecular trans-sialidase, FEBS Lett. 582 (2008) 3348-3352.
45. H. Hashimoto, Recent structural studies of carbohydrate-binding modules, Cell. Mol. Life Sci. 63 (2006) 2954-2967. (Pubitemid 46072301)