A homology model of Xyloglucan Xylosyltransferase 2 reveals critical amino acids involved in substrate binding

Glycobiology

Volumn 26, Issue 9, 2016, Pages 961-972

  Culbertson, Alan T ^a   Tietze, Alesia A ^b   Tietze, Daniel ^b   Chou, Yi Hsiang ^a   Smith, Adrienne L ^a   Young, Zachary T ^a   Zabotina, Olga A ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

glycosyltransferase; homology modeling; plant cell wall; xyloglucan

Indexed keywords

AMINO ACID; ASPARTIC ACID; GLUCAN; GLYCOSYLTRANSFERASE; LYSINE; SERINE; TRANSFERASE; UNCLASSIFIED DRUG; XYLOGLUCAN XYLOSYLTRANSFERASE 2; PROTEIN BINDING; XYLAN; XYLOGLUCAN; XYLOGLUCAN XYLOSYLTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; ENZYME ACTIVITY; ENZYME BINDING; ENZYME LOCALIZATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; ARABIDOPSIS; BINDING SITE; BIOSYNTHESIS; CELL WALL; CHEMISTRY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; MOLECULAR MODEL; PROTEIN CONFORMATION; STRUCTURAL HOMOLOGY;

AMINO ACID SEQUENCE; AMINO ACIDS; ARABIDOPSIS; BINDING SITES; CATALYTIC DOMAIN; CELL WALL; GLUCANS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PENTOSYLTRANSFERASES; PROTEIN BINDING; PROTEIN CONFORMATION; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; XYLANS;

EID: 84991010663     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cww050     Document Type: Article

References (53)

1. Ade CP, Bemm F, Dickson JM, Walter C, Harris PJ. (2014). Family 34 glycosyltransferase (GT34) genes and proteins in Pinus radiata (radiata pine) and Pinus taeda (loblolly pine). Plant J. 78:305-318.
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Boyken SE, Fulton DB, Andreotti AH. (2012). Rescue of the aggregation prone Itk Pleckstrin Homology domain by two mutations derived from the related kinases, Btk and Tec. Protein Sci. 21:1288-1297.
4. Busch C, Hofmann F, Selzer J, Munro S, Jeckel D, Aktories K. (1998). A common motif of eukaryotic glycosyltransferases is essential for the enzyme activity of large clostridial cytotoxins. J Biol Chem. 273:19566-19572.
5. Campbell J, Davies G, Bulone V, Henrissat B. (1997). A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. J Biochem. 326:929-939.
6. Canutescu AA, Shelenkov AA, Dunbrack RL, Jr. (2003). A graph theory algorithm for rapid protein side chain prediction. Protein Sci. 12:2001-2014.
7. Carpita NC. (2012). Progress in the biological synthesis of the plant cell wall: new ideas for improving biomass for bioenergy. Curr Opin Biotechnol. 23:330-337.
8. Carpita NC, Gibeaut DM. (1993). Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3:1-30.
9. Cavalier DM, Keegstra K. (2006). Two xyloglucan xylosyltransferases catalyze the addition of multiple xylosyl residues to cellohexaose. J Biol Chem. 281:34197-34207.
10. Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, et al. (2008). Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell. 20:1519-1537.
11. Chou Y, Pogorelko G, Young ZT, Zabotina OA. (2015). Protein-protein interactions among xyloglucan-synthesizing enzymes and formation of golgilocalized multiprotein complexes. Plant Cell Physiol. 56:255-267
12. Chou YH, Pogorelko G, Zabotina OA. (2012). Xyloglucan xylosyltransferases XXT1, XXT2, and XXT5 and the glucan synthase CSLC4 form Golgilocalized multiprotein complexes. Plant Physiol. 159:1355-1366.
13. Clough SJ, Bent AF. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735-743.
14. Cocuron JC, Lerouxel O, Drakakaki G, Alonso AP, Liepman AH, Keegstra K, Raikhel N, Wilkerson CG. (2007). A gene from the cellulose synthaselike C family encodes a β-1, 4 glucan synthase. Proc Natl Acad Sci. 104:8550-8555.
15. Coutinho PM, Deleury E, Davies GJ, Henrissat B. (2003). An evolving hierarchical family classification for glycosyltransferases. J Mol Biol. 328:307-317.
16. Drozdetskiy A, Cole C, Procter J, Barton GJ. (2015). JPred4: A protein secondary structure prediction server. Nucleic Acids Res. 43(W1), W389-W394.
17. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. (1995). A smooth particle mesh Ewald method. J Chem Phys. 103:8577-8593.
18. Faik A, Price NJ, Raikhel NV, Keegstra K. (2002). An Arabidopsis gene encoding an a-xylosyltransferase involved in xyloglucan biosynthesis. Proc Natl Acad Sci. 99:7797-7802.
19. Gibbons BJ, Roach PJ, Hurley TD. (2002). Crystal structure of the autocatalytic initiator of glycogen biosynthesis, glycogenin. J Mol Biol. 319:463-477.
20. Gloster TM. (2014). Advances in understanding glycosyltransferases from a structural perspective. Curr Opin Struct Biol. 28:131-141.
21. Gotting C, Muller S, Schottler M, Schon S, Prante C, Brinkmann T, Kuhn J, Kleesiek K. (2004). Analysis of the DXD motifs in human xylosyltransferase I required for enzyme activity. J Biol Chem. 279:42566-42573.
22. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R. (2010). A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 38:W695-699.
23. Grubmüller H, Tavan P. (1998). Multiple time step algorithms for molecular dynamics simulations of proteins: How good are they?. J Comput Chem. 19(13):1534-1552
24. Hayashi T. (1989). Xyloglucans in the primary cell wall. Annu Rev Plant Biol. 40:139-168.
25. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. (2006). Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins. 65:712-725.
26. Johal AR, Blackler RJ, Alfaro JA, Schuman B, Borisova S, Evans SV. (2014). pH-induced conformational changes in human ABO(H) blood group glycosyltransferases confirm the importance of electrostatic interactions in the formation of the semi-closed state. Glycobiology. 24:237-246.
27. Konagurthu AS, Whisstock JC, Stuckey PJ, Lesk AM. (2006). MUSTANG: A multiple structural alignment algorithm. Proteins. 64:559-574.
28. Krieger E, Dunbrack RLJr., Hooft RW, Krieger B. (2012). Assignment of protonation states in proteins and ligands: Combining pKa prediction with hydrogen bonding network optimization. Methods Mol Biol. 819:405-421.
29. Krieger E, Joo K, Lee J, Lee J, Raman S, Thompson J, Tyka M, Baker D, Karplus K. (2009). Improving physical realism, stereochemistry, and sidechain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins. 77:114-122.
30. Krieger E, Nielsen JE, Spronk CA, Vriend G. (2006). Fast empirical pKa prediction by Ewald summation. J Mol Graph Model. 25:481-486.
31. Krieger E, Vriend G. (2014). YASARA view-molecular graphics for all devices-from smartphones to workstations. Bioinformatics. 30:2981-2982.
32. Krieger E, Vriend G. (2015). New ways to boost molecular dynamics simulations. J Comput Chem. 36:996-1007.
33. Lairson LL, Henrissat B, Davies GJ, Withers SG. (2008). Glycosyltransferases: Structures, functions, and mechanisms. Annu Rev Biochem. 77:521-555.
34. Laskowski RA. (2009). PDBsum new things. Nucleic Acids Res. 37:D355-359.
35. Li J, Rancour DM, Allende ML, Worth CA, Darling DS, Gilbert JB, Menon AK, Young WWJr. (2001). The DXD motif is required for GM2 synthase activity but is not critical for nucleotide binding. Glycobiology. 11:217-229.
36. Li P, Roberts BP, Chakravorty DK, Merz KMJr. (2013). Rational design of particle mesh Ewald compatible Lennard-Jones parameters for +2 metal cations in explicit solvent. J Chem Theory Comput. 9:2733-2748.
37. Liu J, Mushegian A. (2003). Three monophyletic superfamilies account for the majority of the known glycosyltransferases. Protein Sci. 12:1418-1431.
38. Lobsanov YD, Romero PA, Sleno B, Yu B, Yip P, Herscovics A, Howell PL. (2004). Structure of Kre2p/Mnt1p: A yeast alpha1, 2-mannosyltransferase involved in mannoprotein biosynthesis. J Biol Chem. 279:17921-17931.
39. Madson M. (2003). The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell. 15:1662-1670.
40. Maier JA, Martinez C, Kasavajhala K, Wickstrom L, Hauser KE, Simmerling C. (2015). ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB. J Chem Theory Comput. 11:3696-3713.
41. Mansoori N, Schultink A, Schubert J, Pauly M. (2015). Expression of heterologous xyloglucan xylosyltransferases in Arabidopsis to investigate their role in determining xyloglucan xylosylation substitution patterns. Planta. 241:1145-1158.
42. Park YB, Cosgrove DJ. (2015). Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol. 56:180-194.
43. Pauly M, Keegstra K. (2008). Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J. 54:559-568.
44. Schultink A, Cheng K, Park YB, Cosgrove DJ, Pauly M. (2013). The identification of two arabinosyltransferases from tomato reveals functional equivalency of xyloglucan side chain substituents. Plant Physiol. 163:86-94.
45. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, et al. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 7:539.
46. Stewart JJ. (1990). MOPAC: A semiempirical molecular orbital program. J Comput Aided Mol Des. 4:1-105.
47. Wang C, Li S, Ng S, Zhang B, Zhou Y, Whelan J, Wu P, Shou H. (2014). Mutation in xyloglucan 6-xylosytransferase results in abnormal root hair development in Oryza sativa. J Exp Bot. 65:4149-4157.
48. Wiggins CA, Munro S. (1998). Activity of the yeast MNN1 a-1, 3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc Natl Acad Sci. 95:7945-7950.
49. Zabotina OA. (2012). Xyloglucan and its biosynthesis. Front Plant Sci. 3:134.
50. Zabotina OA, Avci U, Cavalier D, Pattathil S, Chou YH, Eberhard S, Danhof L, Keegstra K, Hahn MG. (2012). Mutations in multiple XXT genes of Arabidopsis reveal the complexity of xyloglucan biosynthesis. Plant Physiol. 159:1367-1384.
51. Zabotina OA, van de Ven WT, Freshour G, Drakakaki G, Cavalier D, Mouille G, Hahn MG, Keegstra K, Raikhel NV. (2008). Arabidopsis XXT5 gene encodes a putative a-1, 6-xylosyltransferase that is involved in xyloglucan biosynthesis. Plant J. 56:101-115.
52. Zhang Y, Wang PG, Brew K. (2001). Specificity and mechanism of metal ion activation in UDP-galactose:β-galactoside-A-1, 3-galactosyltransferase. J Biol Chem. 276:11567-11574.
53. Zhang Y, Xiang Y, Van Etten JL, Rossmann MG. (2007). Structure and function of a chlorella virus-encoded glycosyltransferase. Structure. 15:1031-1039.