Helicobacter hepaticus Hh0072 gene encodes a novel α1-3- fucosyltransferase belonging to CAZy GT11 family

Glycobiology

Volumn 20, Issue 9, 2010, Pages 1077-1088

  Zhang, Lei ^a   Lau, Kam ^a   Cheng, Jiansong ^a,c   Yu, Hai ^a   Li, Yanhong ^a   Sugiarto, Go ^a   Huang, Shengshu ^a   Ding, Li ^a   Thon, Vireak ^a   Wang, Peng G ^b   Chen, Xi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c NANKAI UNIVERSITY   (China)

Author keywords

cloning; fucosyltransferase; Helicobacter hepaticus; Lewis x; sialyl Lewis x

Indexed keywords

ALPHA1 2 FUCOSYLTRANSFERASE; ALPHA1 3 FUCOSYLTRANSFERASE; ALPHA1 4 FUCOSYLTRANSFERASE; GLYCOSYLTRANSFERASE; SIALYL LEWIS X ANTIGEN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; CATALYST; ENZYME ACTIVITY; ENZYME SYNTHESIS; HELICOBACTER HEPATICUS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; CLONING, MOLECULAR; FUCOSYLTRANSFERASES; GLYCOSYLTRANSFERASES; HELICOBACTER HEPATICUS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

HELICOBACTER HEPATICUS;

EID: 77955459001     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwq068     Document Type: Article

References (71)

1. Apoil PA, Roubinet F, Despiau S, Mollicone R, Oriol R, Blancher A. 2000. Evolution of alpha 2-fucosyltransferase genes in primates: relation between an intronic Alu-Y element and red cell expression of ABH antigens. Mol Biol Evol. 17:337-351.
2. Barreaud JP, Saunier K, Souchaire J, Delourme D, Oulmouden A, Oriol R, Leveziel H, Julien R, Petit JM. 2000. Three bovine alpha2-fucosyltransfer-ase genes encode enzymes that preferentially transfer fucose on Galbeta1-3GalNAc acceptor substrates. Glycobiology. 10:611-621.
3. Belot F, Rabuka D, Fukuda M, Hindsgaul O. 2002. Chemoenzymatic synthesis of sulfated O-linked oligosaccharides: epitopes for MECA-79. Tetrahedron Lett. 43:7743-7747.
4. Borges BN, Paiva TS, Harada ML. 2008. Evolution of the SEC1 gene in New World monkey lineages (Primates, Platyrrhini). Genet Mol Res. 7:663-678.
5. Bowman KG, Cook BN, de Graffenried CL, Bertozzi CR. 2001. Biosynthesis of L-selectin ligands: sulfation of sialyl Lewis x-related oligosaccharides by a family of GlcNAc-6-sulfotransferases. Biochemistry. 40:5382-5391.
6. Breton C, Snajdrova L, Jeanneau C, Koca J, Imberty A. 2006. Structures and mechanisms of glycosyltransferases. Glycobiology. 16:29R-37R.
7. Brzezinski K, Stepkowski T, Panjikar S, Bujacz G, Jaskolski M. 2007. High-resolution structure of NodZ fucosyltransferase involved in the biosynthesis of the nodulation factor. Acta Biochim Pol. 54:537-549.
8. Bureau V, Marionneau S, Cailleau-Thomas A, Le Moullac-Vaidye B, Liehr T, Le Pendu J. 2001. Comparison of the three rat GDP-L-fucose:beta-D-galac-toside 2-alpha-L-fucosyltransferases FTA, FTB and FTC. Eur J Biochem. 268:1006-1019.
9. Cahill RJ, Foltz CJ, Fox JG, Dangler CA, Powrie F, Schauer DB. 1997. Inflammatory bowel disease: an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus. Infect Immun. 65:3126-3131.
10. Campbell JA, Davies GJ, Bulone V, Henrissat B. 1997. A classification of nu-cleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem J. 326(Pt 3):929-939.
11. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37:D233-D238.
12. Chan NW, Stangier K, Sherburne R, Taylor DE, Zhang Y, Dovichi NJ, Palcic MM. 1995. The biosynthesis of Lewis X in Helicobacter pylori. Glycobiol-ogy. 5:683-688.
13. Chokhawala HA, Huang S, Lau K, Yu H, Cheng J, Thon V, Hurtado-Ziola N, Guerrero JA, Varki A, Chen X. 2008. Combinatorial chemoenzymatic synthesis and high-throughput screening of sialosides. ACS Chem Biol. 3: 567-576.
14. Coutinho PM, Deleury E, Davies GJ, Henrissat B. 2003. An evolving hierarchical family classification for glycosyltransferases. J Mol Biol. 328:307-317.
15. Daines DA, Wright LF, Chaffin DO, Rubens CE, Silver RP. 2000. NeuD plays a role in the synthesis of sialic acid in Escherichia coli K1. FEMS Microbiol Lett. 189:281-284.
16. Danishefsky SJ, Allen JR. 2000. From the laboratory to the clinic: a retrospective on fully synthetic carbohydrate-based anticancer vaccines frequently used abbreviations are listed in the appendix. Angew Chem Int Ed Engl. 39:836-863.
17. Domino SE, Zhang L, Lowe JB. 2001. Molecular cloning, genomic mapping, and expression of two secretor blood group alpha (1, 2)fucosyltransferase genes differentially regulated in mouse uterine epithelium and gastrointestinal tract. J Biol Chem. 276:23748-23756.
18. Dube DH, Bertozzi CR. 2005. Glycans in cancer and inflammation-potential for therapeutics and diagnostics. Nat Rev Drug Discov. 4:477-488.
19. Fox JG, Dewhirst FE, Tully JG, Paster BJ, Yan L, Taylor NS, Collins MJ Jr, Gorelick PL, Ward JM. 1994. Helicobacter hepaticus sp. nov., a microaer-ophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J Clin Microbiol. 32:1238-1245.
20. Ge Z, Chan NW, Palcic MM, Taylor DE. 1997. Cloning and heterologous expression of an alpha1, 3-fucosyltransferase gene from the gastric pathogen Helicobacter pylori. J Biol Chem. 272:21357-21363.
21. Guo H, Yi W, Shao J, Lu Y, Zhang W, Song J, Wang PG. 2005. Molecular analysis of the O-antigen gene cluster of Escherichia coli O86:B7 and characterization of the chain length determinant gene (wzz). Appl Environ Microbiol. 71:7995-8001.
22. Ichikawa Y, Lin YC, Dumas DP, Shen GJ, Garciajunceda E, Williams MA, Bayer R, Ketcham C, Walker LE, Paulson JC, et al. 1992. Chemical-enzymatic synthesis and conformational-analysis of sialyl Lewis-X and derivatives. J Am Chem Soc. 114:9283-9298.
23. Ihara H, Ikeda Y, Toma S, Wang X, Suzuki T, Gu J, Miyoshi E, Tsukihara T, Honke K, Matsumoto A, et al. 2007. Crystal structure of mammalian alpha1, 6-fucosyltransferase, FUT8. Glycobiology. 17:455-466.
24. Kannagi R. 2002. Regulatory roles of carbohydrate ligands for selectins in the homing of lymphocytes. Curr Opin Struct Biol. 12:599-608.
25. Kannagi R. 2004. Molecular mechanism for cancer-associated induction of sialyl Lewis X and sialyl Lewis A expression-the Warburg effect revisited. Glycoconj J. 20:353-364.
26. Kapust RB, Waugh DS. 1999. Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused. Protein Sci. 8:1668-1674.
27. Kelly RJ, Rouquier S, Giorgi D, Lennon GG, Lowe JB. 1995. Sequence and expression of a candidate for the human Secretor blood group alpha(1, 2) fucosyltransferase gene (FUT2). Homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype. J Biol Chem. 270:4640-4649.
28. Koda Y, Soejima M, Wang B, Kimura H. 1997. Structure and expression of the gene encoding secretor-type galactoside 2-alpha-L-fucosyltransferase (FUT2). Eur J Biochem. 246:750-755.
29. Kudo T, Iwasaki H, Nishihara S, Shinya N, Ando T, Narimatsu I, Narimatsu H. 1996. Molecular genetic analysis of the human Lewis histo-blood group system. II. Secretor gene inactivation by a novel single missense mutation A385T in Japanese nonsecretor individuals. J Biol Chem. 271:9830-9837.
30. Larsen RD, Ernst LK, Nair RP, Lowe JB. 1990. Molecular cloning, sequence, and expression of a human GDP-L-fucose:beta-D-galactoside 2-alpha-L- fucosyltransferase cDNA that can form the H blood group antigen. Proc Natl Acad Sci USA. 87:6674-6678.
31. Li M, Liu XW, Shao J, Shen J, Jia Q, Yi W, Song JK, Woodward R, Chow CS, Wang PG. 2008. Characterization of a novel alpha 1, 2-fucosyltransferase of Escherichia coli O128:B12 and functional investigation of its common motif. Biochemistry. 47:378-387.
32. Lin B, Hayashi Y, Saito M, Sakakibara Y, Yanagisawa M, Iwamori M. 2000. GDP-fucose: beta-galactoside alpha1, 2-fucosyltransferase, MFUT-II, and not MFUT-I or-III, is induced in a restricted region of the digestive tract of germ-free mice by host-microbe interactions and cycloheximide. Biochim Biophys Acta. 1487:275-285.
33. Lin SW, Yuan TM, Li JR, Lin CH. 2006. Carboxyl terminus of Helicobacter pylori alpha1, 3-fucosyltransferase determines the structure and stability. Biochemistry. 45:8108-8116.
34. Lowe JB. 2003. Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr Opin Cell Biol. 15:531-538.
35. Lubineau A, Auge C, Le Goff N, Le Narvor C. 1997. Chemoenzymatic synthesis of a 3IV, 6III-disulfated Lewis(x) pentasaccharide, a candidate ligand for human L-selectin. Carbohydr Res. 305:501-509.
36. Lubineau A, Le Narvor C, Auge C, Gallet PF, Petit JM, Julien R. 1998. Che-mo-enzymatic synthesis of a selectin ligand using recombinant yeast cells. J Mol Catalysis B: Enzymatic. 5:229-234.
37. Ma B, Lau LH, Palcic MM, Hazes B, Taylor ED. 2005. A single aromatic ami-no acid at the carboxyl terminus of Helicobacter pylori alpha1, 3/4 fucosyltransferase determines substrate specificity. J Biol Chem. 280: 36848-36856.
38. Ma B, Simala-Grant JL, Taylor ED. 2006. Fucosylation in prokaryotes and eu-karyotes. Glycobiology. 16:158R-184R.
39. Ma B, Wang G, Palcic MM, Hazes B, Taylor DE. 2003. C-terminal amino acids of Helicobacter pylori alpha1, 3/4 fucosyltransferases determine type I and type II transfer. J Biol Chem. 278:21893-21900.
40. Magnani JL. 2004. The discovery, biology, and drug development of sialyl Lea and sialyl Lex. Arch Biochem Biophys. 426:122-131.
41. Marques ET Jr, Weiss JB, Strand M. 1998. Molecular characterization of a fu-cosyltransferase encoded by Schistosoma mansoni. Mol Biochem Parasitol. 93:237-250.
42. Miyoshi E, Moriwaki K, Nakagawa T. 2008. Biological function of fucosyla-tion in cancer biology. J Biochem. 143:725-729.
43. Monteiro MA, Chan KH, Rasko DA, Taylor DE, Zheng PY, Appelmelk BJ, Wirth HP, Yang M, Blaser MJ, Hynes SO, et al. 1998. Simultaneous expression of type 1 and type 2 Lewis blood group antigens by Helicobacter pylori lipopolysaccharides. Molecular mimicry between H. pylori lipopolysacchar-ides and human gastric epithelial cell surface glycoforms. J Biol Chem. 273:11533-11543.
44. Moran AP. 2008. Relevance of fucosylation and Lewis antigen expression in the bacterial gastroduodenal pathogen Helicobacter pylori. Carbohydr Res. 343:1952-1965.
45. Moran AP, Prendergast MM, Appelmelk BJ. 1996. Molecular mimicry of host structures by bacterial lipopolysaccharides and its contribution to disease. FEMS Immunol Med Microbiol. 16:105-115.
46. Okajima T, Matsuura A, Matsuda T. 2008. Biological functions of glycosyl-transferase genes involved in O-fucose glycan synthesis. J Biochem. 144:1-6.
47. Ouerfelli O, Warren JD, Wilson RM, Danishefsky SJ. 2005. Synthetic carbohydrate-based antitumor vaccines: challenges and opportunities. Expert Rev Vaccines. 4:677-685.
48. Piau JP, Labarriere N, Dabouis G, Denis MG. 1994. Evidence for two distinct alpha(1, 2)-fucosyltransferase genes differentially expressed throughout the rat colon. Biochem J. 300(Pt 3):623-626.
49. Pratt MR, Bertozzi CR. 2004. Syntheses of 6-sulfo sialyl Lewis X gly-cans corresponding to the L-selectin ligand "sulfoadhesin". Org Lett. 6: 2345-2348.
50. Rabbani S, Miksa V, Wipf B, Ernst B. 2005. Molecular cloning and functional expression of a novel Helicobacter pylori alpha-1, 4 fucosyltransferase. Glycobiology. 15:1076-1083.
51. Rogers AB, Fox JG 2004. Inflammation and cancer. I. Rodent models of infectious gastrointestinal and liver cancer. Am J Physiol Gastrointest Liver Physiol. 286:G361-G366.
52. Rouquier S, Lowe JB, Kelly RJ, Fertitta AL, Lennon GG, Giorgi D. 1995. Molecular cloning of a human genomic region containing the H blood group alpha(1, 2)fucosyltransferase gene and two H locus-related DNA restriction fragments. Isolation of a candidate for the human Secretor blood group locus. J Biol Chem. 270:4632-4639.
53. Sanabria-Valentin E, Colbert MT, Blaser MJ. 2007. Role of futC slipped strand mispairing in Helicobacter pylori Lewisy phase variation. Microbes Infect. 9:1553-1560.
54. Saunier K, Barreaud JP, Eggen A, Oriol R, Leveziel H, Julien R, Petit JM. 2001. Organization of the bovine alpha 2-fucosyltransferase gene cluster suggests that the Sec1 gene might have been shaped through a nonautono-mous L1-retrotransposition event within the same locus. Mol Biol Evol. 18:2083-2091.
55. Seeberger PH, Werz DB. 2007. Synthesis and medical applications of oligosaccharides. Nature. 446:1046-1051.
56. Shao J, Li M, Jia Q, Lu Y, Wang PG 2003. Sequence of Escherichia coli O128 antigen biosynthesis cluster and functional identification of an alpha-1, 2-fucosyltransferase. FEBSLett. 553:99-103.
57. Simanek EE, McGarvey GJ, Jablonowski JA, Wong CH. 1998. Selectin-carbohydrate interactions: From natural ligands to designed mimics. Chem Rev. 98:833-862.
58. Smialowski P, Martin-Galiano AJ, Mikolajka A, Girschick T, Holak TA, Frishman D. 2007. Protein solubility: sequence based prediction and experimental verification. Bioinformatics. 23:2536-2542.
59. Suerbaum S, Josenhans C, et al. 2003. The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc Natl Acad Sci USA. 100:7901-7906.
60. Suerbaum S, Michetti P. 2002. Helicobacter pylori infection. N Engl J Med. 347:1175-1186.
61. 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.
62. Timmons SC, Jakeman DL. 2007. Stereoselective chemical synthesis of sugar nucleotides via direct displacement of acylated glycosyl bromides. Org Lett. 9:1227-1230.
63. van Der Wel H, Morris HR, Panico M, Paxton T, North SJ, Dell A, Thomson JM, West CM. 2001. A non-Golgi alpha 1, 2-fucosyltransferase that modifies Skp1 in the cytoplasm of Dictyostelium. J Biol Chem. 276:33952-33963.
64. Wang G, Boulton PG, Chan NW, Palcic MM, Taylor DE. 1999. Novel Helicobacter pylori alpha1, 2-fucosyltransferase, a key enzyme in the synthesis of Lewis antigens. Microbiology. 145(Pt 11):3245-3253.
65. Wang G, Ge Z, Rasko DA, Taylor DE. 2000. Lewis antigens in Helicobacter pylori: biosynthesis and phase variation. Mol Microbiol. 36:1187-1196.
66. Wang W, Hu T, Frantom PA, Zheng T, Gerwe B, Del Amo DS, Garret S, Seidel RD 3rd, Wu P. 2009. Chemoenzymatic synthesis of GDP-L-fucose and the Lewis X glycan derivatives. Proc Natl Acad Sci USA. 106:16096-16101.
67. Yi W, Liu X, Li Y, Li J, Xia C, Zhou G, Zhang W, Zhao W, Chen X, Wang PG. 2009. Remodeling bacterial polysaccharides by metabolic pathway engineering. Proc Natl Acad Sci USA. 106:4207-4212.
68. Yu H, Cheng J, Ding L, Khedri Z, Chen Y, Chin S, Lau K, Tiwari VK, Chen X. 2009. Chemoenzymatic synthesis of GD3 oligosaccharides and other disia-lyl glycans containing natural and non-natural sialic acids. J Am Chem Soc. 131:18467-18477.
69. Yu H, Chokhawala H, Karpel R, Yu H, Wu B, Zhang J, Zhang Y, Jia Q, Chen X. 2005. A multifunctional Pasteurella multocida sialyltransferase: a powerful tool for the synthesis of sialoside libraries. J Am Chem Soc. 127: 17618-17619.
70. Yu H, Yu H, Karpel R, Chen X. 2004. Chemoenzymatic synthesis of CMP-sialic acid derivatives by a one-pot two-enzyme system: comparison of substrate flexibility of three microbial CMP-sialic acid synthetases. Bioorg Med Chem. 12:6427-6435.
71. Zheng Q, Van Die I, Cummings RD. 2008. A novel alpha1, 2-fucosyltransfer-ase (CE2FT-2) in Caenorhabditis elegans generates H-type 3 glycan structures. Glycobiology. 18:290-302.