High-resolution structure of NodZ fucosyltransferase involved in the biosynthesis of the nodulation factor

Acta Biochimica Polonica

Volumn 54, Issue 3, 2007, Pages 537-549

  Brzezinski, Krzysztof ^a   Stepkowski, Tomasz ^b   Panjikar, Santosh ^c   Bujacz, Grzegorz ^b,d   Jaskolski, Mariusz ^a,b  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

^b POLISH ACADEMY OF SCIENCES   (Poland)

^c DESY   (Germany)

^d LODZ UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

Fucosyltransferase; Glycosyltransferase; Nitrogen fixation; Nodulation; NodZ

Indexed keywords

BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM; ESCHERICHIA COLI;

EID: 35348893812     PISSN: 0001527X     EISSN: 1734154X     Source Type: Journal    
DOI: 10.18388/abp.2007_3227     Document Type: Article

References (58)

1. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98: 10037-10041.
2. Bond CS (2003) TopDraw: a sketchpad for protein structure topology cartoons. Bioinformatics 19: 311-312.
3. Breton C, Oriol R, Imberty A (1998) Conserved structural features in eukaryotic and prokaryotic fucosyltransferases. Glycobiology 8: 87-94.
4. Brzezinski K, Rogozinski B, Stepkowski T, Bujacz G, Jaskolski M (2004) Cloning, purification, crystallization and preliminary crystallographic studies of Bradyrhizobium fucosyltransferase NodZ. Acta Cryst D60: 344-346.
5. Campbell RE, Mosimann SC, Tanner ME, Strynadka NCJ (2000) The structure of UDP-N-acetylglucosamine 2-epimerase reveals homology to phosphoglycosyl transferase. Biochemistry 39: 14993-15001.
6. Charnock SJ, Davies GJ (1999) Structure of the nucleotidediphospho-sugar transferase, SpsA from Bacillus subtilis, in native and nucleotide-complexed forms. Biochemistry 38: 6380-6385.
7. Chazalet V, Uehara K, Geremia RA, Breton C (2001) Identification of essential amino acids in the Azorhizobium caulinodans fucosyltransferase NodZ. J Bacteriol 183: 7067-7075.
8. Cid E, Gomis RR, Geremia RA, Guinovart JJ, Ferrer JC (2000) Identification of two essential glutamic acid residues in glycogen synthase. J Biol Chem 275: 33614-33621.
9. Cohen GE (1997) ALIGN: a program to superimpose protein coordinates, accounting for insertions and deletions. J Appl Cryst 30: 1160-1161.
10. Coutinho PM, Henrissat B (1999) Carbohydrate-active enzymes: an integrated database approach. In Recent Advances in Carbohydrate Bioengineering (Gilbert HJ, Davies G, Henrissat B, Svensson B, eds) pp 3-12. The Royal Society of Chemistry, Cambridge.
11. Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328: 307-317.
12. Davies GJ, Gloster TM, Henrissat B (2005) Recent structural insights into the expanding world of carbohydrateactive enzymes. Curr Opin Struct Biol 15: 637-645.
13. Debelle F, Moulin L, Mangin B, Denarie J, Boivin C (2001) nod Genes and Nod signals and the evolution of the rhizobium legume symbiosis. Acta Biochim Polon 48: 359-365.
14. Denarie J, Debelle F, Prome JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503-535.
15. Gibson RP, Tarling CA, Roberts S, Withers SG, Davies GJ (2004) The donor subsite of trehalose-6-phosphate synthase: binary complexes with UDP-glucose and UDP-2-deoxy-2-fluoro-glucose at 2 Å resolution. J Biol Chem 279: 1950-1955.
16. Ha S, Walker D, Shi Y, Walker S (2000) The 1.9 Å crystal structure of Escherichia coli MurG, a membrane-associated glycosyltransferase involved in peptidoglycan biosynthesis. Protein Sci 9: 1045-1052.
17. Henrissat B, Davies G (2000) Glycoside hydrolases and glycosyltransferases. Families, modules, and implications for genomics. Plant Physiol 124: 1515-1519.
18. Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
19. Holm L, Sander C (1998) Touring protein fold space with Dali/FSSP. Nucleic Acids Res 26: 316-319.
20. Ihara H, Ikeda Y, Taniguchi N (2006) Reaction mechanism and substrate specificity for nucleotide sugar of mammalian α1,6-fucosyltransferase - a large-scale preparation and characterization of recombinant human FUT8. Glycobiology 16: 333-342.
21. Ihara H, Ikeda Y, Toma S, Wang X, Suzuki T, Gu J, Miyoshi E, Tsukihara T, Honke K, Matsumoto A, Nakagawa A, Taniguchi N (2007) Crystal structure of mammalian α1,6-fucosyltransferase, FUT8. Glycobiology 17: 455-466.
22. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
23. Lariviere L, Sommer N, Morera S (2005) Structural evidence of a passive base-flipping mechanism for AGT, an unusual GT-B glycosyltransferase. J Mol Biol 352: 139-150.
24. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26: 283-291.
25. Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol 54: 575-594.
26. Ma B, Simala-Grant JL, Taylor DE (2006) Fucosylation in prokaryotes and eukaryotes. Glycobiology 16: 158R-184R.
27. Martinez-Duncker I, Michalski JC, Bauvy C, Candelier JJ, Mennesson B, Codogn P, Oriol R, Mollicone R (2003) A new superfamily of protein-O- fucosyltransferases, α2-fucosyltransferases, and α6- fucosyltransferases: phylogeny and identification of conserved peptide motifs. Glycobiology 13: 1C-5C.
28. Martinez-Fleites C, Proctor M, Roberts S, Bolam DN, Gilbert HJ, Davies GJ (2006) Insights into the synthesis of lipopolysaccharide and antibiotics through the structures of two retaining glycosyltransferases from family GT4. Chem Biol 13: 1143-1152.
29. McRee DE (1999) XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125: 156-165.
30. Mergaert P, D'Haeze W, Fernandez-Lopez M, Geelen D, Goethals K, Prome JC, van Montagu M, Holsters M (1996) Fucosylation and arabinosylation of Nod factors in Azorhizobium caulinodans: involvement of nolK, nodZ as well as noeC and/or downstream genes. Mol Microbiol 21: 409-419.
31. Morera S, Imberty A, Aschke-Sonnenborn U, Ruger W, Freemont PS (1999) T4 phage β-glucosyltransferase: substrate binding and proposed catalytic mechanism. J Mol Biol 292: 717-730.
32. Morris RJ, Zwart PH, Cohen S, Fernandez FJ, Kakaris M, Kirillova O, Vonrhein C, Perrakis A, Lamzin VS (2004) Breaking good resolutions with ARP/wARP. J Synchrotron Rad 11: 56-59.
33. Mulichak AM, Losey HC, Walsh CT, Garavito RM (2001) Structure of the UDP-glucosyltransferase GtfB that modifies the heptapeptide aglycone in the biosynthesis of vancomycin group antibiotics. Structure 9: 547-557.
34. Mulichak AM, Lu W, Losey HC, Walsh CT, Garavito RM (2004) Crystal structure of vancosaminyltransferase GtfD from the vancomycin biosynthetic pathway: interactions with acceptor and nucleotide ligands. Biochemistry 43: 5170-5180.
35. Murray BW, Takayama S, Schultz J, Wong CH (1996) Mechanism and specificity of human α-1,3-fucosyltransferase V. Biochemistry 35: 11183-11195.
36. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Cryst D53: 240-255.
37. 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.
38. Offen W, Martinez-Fleites C, Yang M, Kiat-Lim E, Davis BG, Tarling CA, Ford CM, Bowles DJ, Davies GJ (2006) Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO J 25: 1396-1405.
39. Olsthoorn MM, Lopez-Lara IM, Petersen BO, Bock K, Haverkamp J, Spaink HP, Thomas-Oates JE (1998) Novel branched nod factor structure results from α-(1→3) fucosyl transferase activity: the major lipo-chitin oligosaccharides from Mesorhizobium loti strain NZP2213 bear an α-(1→3) fucosyl substituent on a nonterminal backbone residue. Biochemistry 37: 9024-9032.
40. Oriol R, Mollicone R, Cailleau A, Balanzino L, Breton C (1999) Divergent evolution of fucosyltransferases genes from vertebrates, invertebrates and bacteria. Glycobiology 9: 323-334.
41. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
42. Panjikar S, Parthasarathy V, Lamzin VS, Weiss MS, Tucker PA (2005) Auto-Rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Cryst D61: 449-457.
43. Quesada-Vincens D, Fellay R, Nasim T, Viprey V, Burger U, Prome JC, Broughton WJ, Jabbouri S (1997) Rhizobium sp. strain NGR234 NodZ protein is a fucosyltransferase. J Bacteriol 179: 5087-5093.
44. Quinto C, Wijfjes AH, Bloemberg GV, Blok-Tip L, Lopez-Lara IM, Lugtenberg BJ, Thomas-Oates JE, Spaink HP (1997) Bacterial nodulation protein NodZ is a chitin oligosaccharide fucosyltransferase which can also recognize related substrates of animal origin. Proc Natl Acad Sci USA 94: 4336-4341.
45. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21: 541-554.
46. Schneider TR, Sheldrick GM (2002) Substructure solution with SHELXD. Acta Cryst D58: 1772-1779.
47. Shao H, He X, Achnine L, Blount JW, Dixon RA, Wang X (2005) Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. Plant Cell 17: 3141-3154.
48. Sheldrick GM (2002) Macromolecular phasing with SHELXE Z. Kristallogr 217: 644-650.
49. Stacey G, Luka S, Sanjuan J, Banfalvi Z, Nieuwkoop AJ, Chun JY, Forsberg LS, Carlson R (1994) NodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum. J Bacteriol 176: 620-633.
50. Stepkowski T, Legocki AB (2001) Reduction of bacterial genome size and expansion resulting from obligate intracellular lifestyle and adaptation to soil habitat. Acta Biochim Polon 48: 367-384.
51. Stepkowski T, Swiderska A, Miedzinska K, Czaplinska M, Swiderski M, Biesiadka J, Legocki AB (2003) Low sequence similarity and gene content of symbiotic clusters of Bradyrhizobium sp. WM9 (Lupinus) indicate early divergence of "lupin" lineage in the genus Bradyrhizobium. Antonie Van Leeuwenhoek 84: 115-124.
52. Sun HY, Lin SW, Ko TP, Pan JF, Liu CL, Lin CN, Wang AH, Lin CH (2007) Structure and mechanism of Helicobacter pylori fucosyltransferase. A basis for lipopolysaccharide variation and inhibitor design. J Biol Chem 282: 9973-9982.
53. Takahashi T, Ikeda Y, Tateishi A, Yamaguchi Y, Ishikawa M, Taniguchi N (2000) A sequence motif involved in the donor substrate binding by α1,6-fucosyltransferase: the role of the conserved arginine residues. Glycobiology 10: 503-510.
54. Vagin A, Teplyakov A (1997) MOLREP: an automated program for molecular replacement. J Appl Cryst 30: 1022-1025.
55. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 229: 105-124.
56. Vrielink A, Ruger W, Driessen HP, Freemont PS (1994) Crystal structure of the DNA modifying enzyme β-glucosyltransferase in the presence and absence of the substrate uridine diphosphoglucose. EMBO J 13: 3413-3422.
57. Winn MD, Isupov MN, Murshudov GN (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Cryst D57: 122-133.
58. Wrabl JO, Grishin NV (2001) Homology between O-linked GlcNAc transferases and proteins of the glycogen phosphorylase superfamily. J Mol Biol 314: 365-374.