Structure of a novel O-linked N-acetyl-D-glucosamine (O-GlcNAc) transferase, GtfA, reveals insights into the glycosylation of pneumococcal serine-rich repeat adhesins

Journal of Biological Chemistry

Volumn 289, Issue 30, 2014, Pages 20898-20907

  Shi, Wei Wei ^a   Jiang, Yong Liang ^a   Zhu, Fan ^b   Yang, Yi Hu ^a   Shao, Qiu Yan ^a   Yang, Hong Bo ^a   Ren, Yan Min ^a   Wu, Hui ^b   Chen, Yuxing ^a   Zhou, Cong Zhao ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTERIFICATION; GLYCOSYLATION; PROTEINS;

BIOLOGICAL PROCESS; CATALYTIC DOMAINS; N-ACETYL-D-GLUCOSAMINE; PROTEIN GLYCOSYLATION; SERINE RESIDUES; STREPTOCOCCUS PNEUMONIAE; TETRATRICOPEPTIDE REPEATS; UNIVERSAL MECHANISMS;

AMINO ACIDS;

ADHESIN; AMINOTRANSFERASE; MULTIENZYME COMPLEX;

CHEMISTRY; ENZYMOLOGY; GENETICS; GLYCOSYLATION; METABOLISM; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STREPTOCOCCUS PNEUMONIAE; X RAY CRYSTALLOGRAPHY;

ADHESINS, BACTERIAL; CRYSTALLOGRAPHY, X-RAY; GLYCOSYLATION; MULTIENZYME COMPLEXES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; STREPTOCOCCUS PNEUMONIAE; TRANSAMINASES;

EID: 84905408669     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.581934     Document Type: Article

References (61)

1. Drickamer, K., and Taylor, M. E. (1998) Evolving views of protein glycosylation. Trends Biochem. Sci. 23, 321-324
2. Hart, G. W., Slawson, C., Ramirez-Correa, G., and Lagerlof, O. (2011) Cross talk betweenO-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu. Rev. Biochem. 80, 825-858
3. Vaidyanathan, K., Durning, S., and Wells, L. (2014) Functional O-GlcNAc modifications: implications in molecular regulation and pathophysiology. Crit Rev. Biochem. Mol. Biol. 49, 140-163
4. Torres, C. R., and Hart, G. W. (1984) Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes: evidence for O-linked GlcNAc. J. Biol. Chem. 259, 3308-3317
5. Yang, Y. R., and Suh, P. G. (2014) O-GlcNAcylation in cellular functions and human diseases. Adv. Biol. Regul. 54, 68-73
6. Lazarus, M. B., Nam, Y., Jiang, J., Sliz, P., and Walker, S. (2011) Structure of human O-GlcNAc transferase and its complex with a peptide substrate. Nature 469, 564-567
7. Lazarus, M. B., Jiang, J., Gloster, T. M., Zandberg, W. F., Whitworth, G. E., Vocadlo, D. J., and Walker, S. (2012) Structural snapshots of the reaction coordinate for O-GlcNAc transferase. Nat. Chem. Biol. 8, 966-968
8. Martinez-Fleites, C., Macauley, M. S., He, Y., Shen, D. L., Vocadlo, D. J., and Davies, G. J. (2008) Structure of an O-GlcNAc transferase homolog provides insight into intracellular glycosylation. Nat. Struct. Mol. Biol. 15, 764-765
9. Clarke, A. J., Hurtado-Guerrero, R., Pathak, S., Schüttelkopf, A. W., Borodkin, V., Shepherd, S. M., Ibrahim, A. F., and van Aalten, D. M. (2008) Structural insights into mechanism and specificity of O-GlcNAc transferase. EMBO J. 27, 2780-2788
10. Jínek, M., Rehwinkel, J., Lazarus, B. D., Izaurralde, E., Hanover, J. A., and Conti, E. (2004) The superhelical TPR-repeat domain of O-linked GlcNAc transferase exhibits structural similarities to importin α. Nat. Struct. Mol. Biol. 11, 1001-1007
11. Shen, A., Kamp, H. D., Gründling, A., and Higgins, D. E. (2006) A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev. 20, 3283-3295
12. Nothaft, H., and Szymanski, C. M. (2010) Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8, 765-778
13. Kukita, K., Kawada-Matsuo, M., Oho, T., Nagatomo, M., Oogai, Y., Hashimoto, M., Suda, Y., Tanaka, T., and Komatsuzawa, H. (2013) Staphylococcus aureus SasA is responsible for binding to the salivary agglutinin gp340, derived from human saliva. Infect. Immun. 81, 1870-1879
14. Sheen, T. R., Jimenez, A., Wang, N. Y., Banerjee, A., van Sorge, N. M., and Doran, K. S. (2011) Serine-rich repeat proteins and pili promote Streptococcus agalactiae colonization of the vaginal tract. J. Bacteriol. 193, 6834-6842
15. Sanchez, C. J., Shivshankar, P., Stol, K., Trakhtenbroit, S., Sullam, P. M., Sauer, K., Hermans, P. W., and Orihuela, C. J. (2010) The pneumococcal serine-rich repeat protein is an intra-species bacterial adhesin that promotes bacterial aggregation in vivo and in biofilms. PLoS Pathog. 6, e1001044
16. Pyburn, T. M., Bensing, B. A., Xiong, Y. Q., Melancon, B. J., Tomasiak, T. M., Ward, N. J., Yankovskaya, V., Oliver, K. M., Cecchini, G., Sulikowski, G. A., Tyska, M. J., Sullam, P. M., and Iverson, T. M. (2011) A structural model for binding of the serine-rich repeat adhesin GspB to host carbohydrate receptors. PLoS Pathog 7, e1002112
17. King, N. P., Beatson, S. A., Totsika, M., Ulett, G. C., Alm, R. A., Manning, P. A., and Schembri, M. A. (2011) UafB is a serine-rich repeat adhesin of Staphylococcus saprophyticus that mediates binding to fibronectin, fibrinogen, and human uroepithelial cells. Microbiology 157, 1161-1175
18. Lizcano, A., Sanchez, C. J., and Orihuela, C. J. (2012) A role for glycosylated serine-rich repeat proteins in Gram-positive bacterial pathogenesis. Mol. Oral Microbiol. 27, 257-269
19. Zhou, M., and Wu, H. (2009) Glycosylation and biogenesis of a family of serine-rich bacterial adhesins. Microbiology 155, 317-327
20. Takamatsu, D., Bensing, B. A., and Sullam, P. M. (2004) Four proteins encoded in the gspB-secY2A2 operon of Streptococcus gordonii mediate the intracellular glycosylation of the platelet-binding protein GspB. J. Bacteriol. 186, 7100-7111
21. Shivshankar, P., Sanchez, C., Rose, L. F., and Orihuela, C. J. (2009) The Streptococcus pneumoniae adhesin PsrP binds to Keratin 10 on lung cells. Mol. Microbiol. 73, 663-679
22. Hegge, F. T., Hitchen, P. G., Aas, F. E., Kristiansen, H., Løvold, C., Egge-Jacobsen, W., Panico, M., Leong, W. Y., Bull, V., Virji, M., Morris, H. R., Dell, A., and Koomey, M. (2004) Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc. Natl. Acad. Sci. U. S. A. 101, 10798-10803
23. Seepersaud, R., Bensing, B. A., Yen, Y. T., and Sullam, P. M. (2012) The accessory Sec protein Asp2 modulates GlcNAc deposition onto the serinerich repeat glycoprotein GspB. J. Bacteriol. 194, 5564-5575
24. Wu, R., Zhou, M., and Wu, H. (2010) Purification and characterization of an activeN-acetylglucosaminyltransferase enzyme complex from Streptococci. Appl. Environ. Microbiol. 76, 7966-7971
25. Wu, R., and Wu, H. (2011) Amolecular chaperone mediates a two-protein enzyme complex and glycosylation of serine-rich streptococcal adhesins. J. Biol. Chem. 286, 34923-34931
26. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Macromolecular Crystallography 276, 307-326
27. Brodersen, D. E., de La Fortelle, E., Vonrhein, C., Bricogne, G., Nyborg, J., and Kjeldgaard, M. (2000) Applications of single-wavelength anomalous dispersion at high and atomic resolution. Acta Crystallogr. D Biol. Crystallogr. 56, 431-441
28. Sheldrick, G. M. (2008) A short history of SHELX. Acta Crystallogr. A 64, 112-122
29. Hao, Q., Gu, Y. X., Zheng, C. D., and Fan, H. F. (2000) OASIS: a computer program for breaking phase ambiguity in one-wavelength anomalous scattering or single isomorphous substitution (replacement) data. J. Appl. Crystallogr. 33, 980-981
30. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55, 849-861
31. Terwilliger, T. C. (2003) Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr. D Biol. Crystallogr. 59, 38-44
32. Cowtan, K. (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011
33. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
34. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr 53, 240-255
35. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
36. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
37. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
38. Laskowski, R., Macarthur, M., Moss, D., and Thornton, J. (1993) Procheck: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
39. DeLano, W. (2002) The PyMOL Molecular Graphics System, De Lano Scientific, San Carlos CA
40. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
41. Holm, L., and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138
42. Coutinho, P. M., Deleury, E., Davies, G. J., and Henrissat, B. (2003) An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 328, 307-317
43. Ruane, K. M., Davies, G. J., and Martinez-Fleites, C. (2008) Crystal structure of a family GT4 glycosyltransferase from Bacillus anthracis ORF BA1558. Proteins 73, 784-787
44. Parsonage, D., Newton, G. L., Holder, R. C., Wallace, B. D., Paige, C., Hamilton, C. J., Dos Santos, P. C., Redinbo, M. R., Reid, S. D., and Claiborne, A. (2010) Characterization of the N-acetyl-α-D-glucosaminyl lmalate synthase and deacetylase functions for bacillithiol biosynthesis in Bacillus anthracis. Biochemistry 49, 8398-8414
45. Guerin, M. E., Kordulakova, J., Schaeffer, F., Svetlikova, Z., Buschiazzo, A., Giganti, D., Gicquel, B., Mikusova, K., Jackson, M., and Alzari, P. M. (2007) Molecular recognition and interfacial catalysis by the essential phosphatidylinositol mannosyltransferase PimA from mycobacteria. J. Biol. Chem. 282, 20705-20714
46. Vetting, M. W., Frantom, P. A., and Blanchard, J. S. (2008) Structural and enzymatic analysis of MshA from Corynebacterium glutamicum: substrateassisted catalysis. J. Biol. Chem. 283, 15834-15844
47. Hu, Y., Chen, L., Ha, S., Gross, B., Falcone, B., Walker, D., Mokhtarzadeh, M., and Walker, S. (2003) 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, 845-849
48. Buschiazzo, A., Ugalde, J. E., Guerin, M. E., Shepard, W., Ugalde, R. A., and Alzari, P. M. (2004) Crystal structure of glycogen synthase: homologous enzymes catalyze glycogen synthesis and degradation. EMBO J. 23, 3196-3205
49. Cottee, M. A., Muschalik, N., Wong, Y. L., Johnson, C. M., Johnson, S., Andreeva, A., Oegema, K., Lea, S. M., Raff, J. W., and van Breugel, M. (2013) Crystal structures of the CPAP/STIL complex reveal its role in centriole assembly and human microcephaly. Elife 2, e01071
50. Makabe, K., McElheny, D., Tereshko, V., Hilyard, A., Gawlak, G., Yan, S., Koide, A., and Koide, S. (2006) Atomic structures of peptide self-assembly mimics. Proc. Natl. Acad. Sci. U. S. A. 103, 17753-17758
51. Greenwald, J., Nader, M., Celia, H., Gruffaz, C., Geoffroy, V., Meyer, J. M., Schalk, I. J., and Pattus, F. (2009) FpvA bound to non-cognate pyoverdines: molecular basis of siderophore recognition by an iron transporter. Mol. Microbiol. 72, 1246-1259
52. Kawai, F., Grass, S., Kim, Y., Choi, K. J., St Geme, J. W., 3rd, and Yeo, H. J. (2011) Structural insights into the glycosyltransferase activity of the Actinobacillus pleuropneumoniae HMW1C-like protein. J. Biol. Chem. 286, 38546-38557
53. Ihara, H., Ikeda, Y., Toma, S., Wang, X., Suzuki, T., Gu, J., Miyoshi, E., Tsukihara, T., Honke, K., Matsumoto, A., Nakagawa, A., and Taniguchi, N. (2007) Crystal structure of mammalian α1, 6-fucosyltransferase, FUT8. Glycobiology 17, 455-466
54. Kakuta, Y., Okino, N., Kajiwara, H., Ichikawa, M., Takakura, Y., Ito, M., and Yamamoto, T. (2008) 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, 66-73
55. Qasba, P. K., and Ramakrishnan, B. (2007) Letter to the glyco-forum: catalytic domains of glycosyltransferases with "add-on" domains. Glycobiology 17, 7G-9G
56. Dominguez, C., Boelens, R., and Bonvin, A. M. (2003) HADDOCK: a proteinprotein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125, 1731-1737
57. Lairson, L. L., Henrissat, B., Davies, G. J., and Withers, S. G. (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555
58. Gross, B. J., Kraybill, B. C., and Walker, S. (2005) Discovery of O-GlcNAc transferase inhibitors. J. Am. Chem. Soc. 127, 14588-14589
59. Errey, J. C., Lee, S. S., Gibson, R. P., Martinez Fleites, C., Barry, C. S., Jung, P. M., O'Sullivan, A. C., Davis, B. G., and Davies, G. J. (2010) Mechanistic insight into enzymatic glycosyl transfer with retention of configuration through analysis of glycomimetic inhibitors. Angew. Chem. Int. Ed. Engl. 49, 1234-1237
60. Iyer, S. P., and Hart, G. W. (2003) Roles of the tetratricopeptide repeat domain in O-GlcNAc transferase targeting and protein substrate specificity. J. Biol. Chem. 278, 24608-24616
61. Li, Y., Chen, Y., Huang, X., Zhou, M., Wu, R., Dong, S., Pritchard, D. G., Fives-Taylor, P., and Wu, H. (2008) A conserved domain of previously unknown function in Gap1 mediates protein-protein interaction and is required for biogenesis of a serine-rich streptococcal adhesin. Mol. Microbiol. 70, 1094-1104