Characterization of the Caenorhabditis elegans UDP-galactopyranose mutase homolog glf-1 reveals an essential role for galactofuranose metabolism in nematode surface coat synthesis

Developmental Biology

Volumn 335, Issue 2, 2009, Pages 340-355

  Novelli, Jacopo F ^a   Chaudhary, Kshitiz ^a   Canovas, Julie ^a   Benner, Jack S ^a   Madinger, Catherine L ^a   Kelly, Paul ^c   Hodgkin, Jonathan ^b   Carlow, Clotilde K S ^a  

^a NEW ENGLAND BIOLABS   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c SALEM STATE UNIVERSITY   (United States)

Author keywords

C. elegans; Galactofuranose; Glycans; M. nematophilum; Nematodes; Surface coat; UGM

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; GALACTOFURANOSE; GALACTOSE; GLF 1 PROTEIN; GLYCAN; ISOMERASE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GALACTOPYRANOSE MUTASE;

ACTINOMYCETALES; ARTICLE; BACTERIUM ADHERENCE; CAENORHABDITIS ELEGANS; CARBOHYDRATE SYNTHESIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; INFECTION RESISTANCE; LARVAL DEVELOPMENT; LEISHMANIA MAJOR; MICROBACTERIUM NEMATOPHILUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE PHENOMENA AND FUNCTIONS; PARASITE SURVIVAL; PRIORITY JOURNAL; SURFACE COAT;

ANIMALIA; CAENORHABDITIS ELEGANS; EUKARYOTA; LEISHMANIA MAJOR; MICROBACTERIUM NEMATOPHILUM; NEMATODA; PROKARYOTA; PROTOZOA; RHABDITIDA; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GALACTOSE; GENE KNOCKOUT TECHNIQUES; GRAM-POSITIVE BACTERIA; INTRAMOLECULAR TRANSFERASES; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 70350238208     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.09.010     Document Type: Article

References (101)

1. Ashrafi K., Chang F.Y., Watts J.L., Fraser A.G., Kamath R.S., Ahringer J., and Ruvkun G. Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421 (2003) 268-272
2. Bakker H., Kleczka B., Gerardy-Schahn R., and Routier F.H. Identification and partial characterization of two eukaryotic UDP-galactopyranose mutases. Biol. Chem. 386 (2005) 657-661
3. Beis K., Srikannathasan V., Liu H., Fullerton S.W., Bamford V.A., Sanders D.A., Whitfield C., McNeil M.R., and Naismith J.H. Crystal structures of Mycobacteria tuberculosis and Klebsiella pneumoniae UDP-galactopyranose mutase in the oxidised state and Klebsiella pneumoniae UDP-galactopyranose mutase in the (active) reduced state. J. Mol. Biol. 348 (2005) 971-982
4. Belanova M., Dianiskova P., Brennan P.J., Completo G.C., Rose N.L., Lowary T.L., and Mikusova K. Galactosyl transferases in mycobacterial cell wall synthesis. J. Bacteriol. 190 (2008) 1141-1145
5. Berninsone, P.M., (2006). "Carbohydrates and glycosylation." The C. elegans Research Community WormBook, doi:10.1895/wormbook.1.125.1, http://www.wormbook.org.
6. Berninsone P., Hwang H.Y., Zemtseva I., Horvitz H.R., and Hirschberg C.B. SQV-7, a protein involved in Caenorhabditis elegans epithelial invagination and early embryogenesis, transports UDP-glucuronic acid, UDP-N-acetylgalactosamine, and UDP-galactose. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 3738-3743
7. Beverley S.M., Owens K.L., Showalter M., Griffith C.L., Doering T.L., Jones V.C., and McNeil M.R. Eukaryotic UDP-galactopyranose mutase (GLF gene) in microbial and metazoal pathogens. Eukaryot Cell 4 (2005) 1147-1154
8. Bird A.F., and Bird J. The Exoskeleton. In: Press A. (Ed). The structure of nematodes (1991), San Diego
9. Blaxter M.L., Page A.P., Rudin W., and Maizels R.M. Nematode surface coats: actively evading immunity. Parasitol. Today 8 (1992) 243-247
10. Borgonie G., van Driessche E., Link C.D., de Waele D., and Coomans A. Tissue treatment for whole mount internal lectin staining in the nematodes Caenorhabditis elegans, Panagrolaimus superbus and Acrobeloides maximus. Histochemistry 101 (1994) 379-384
11. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
12. Caffaro C.E., Hirschberg C.B., and Berninsone P.M. Independent and simultaneous translocation of two substrates by a nucleotide sugar transporter. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 16176-16181
13. Caffaro C.E., Hirschberg C.B., and Berninsone P.M. Functional redundancy between two Caenorhabditis elegans nucleotide sugar transporters with a novel transport mechanism. J. Biol. Chem. 282 (2007) 27970-27975
14. Caffaro C.E., Luhn K., Bakker H., Vestweber D., Samuelson J., Berninsone P., and Hirschberg C.B. A single Caenorhabditis elegans Golgi apparatus-type transporter of UDP-glucose, UDP-galactose, UDP-N-acetylglucosamine, and UDP-N-acetylgalactosamine. Biochemistry 47 (2008) 4337-4344
15. Carlson E.E., May J.F., and Kiessling L.L. Chemical probes of UDP-galactopyranose mutase. Chem. Biol. 13 (2006) 825-837
16. Chad J.M., Sarathy K.P., Gruber T.D., Addala E., Kiessling L.L., and Sanders D.A. Site-directed mutagenesis of UDP-galactopyranose mutase reveals a critical role for the active-site, conserved arginine residues. Biochemistry 46 (2007) 6723-6732
17. Cipollo J.F., Costello C.E., and Hirschberg C.B. The fine structure of Caenorhabditis elegans N-glycans. J. Biol. Chem. 277 (2002) 49143-49157
18. Cipollo J.F., Awad A.M., Costello C.E., and Hirschberg C.B. srf-3, a mutant of Caenorhabditis elegans, resistant to bacterial infection and to biofilm binding, is deficient in glycoconjugates. J. Biol. Chem. 279 (2004) 52893-52903
19. Damveld R.A., Franken A., Arentshorst M., Punt P.J., Klis F.M., van den Hondel C.A., and Ram A.F. A novel screening method for cell wall mutants in Aspergillus niger identifies UDP-galactopyranose mutase as an important protein in fungal cell wall biosynthesis. Genetics 178 (2008) 873-881
20. Darby C., Chakraborti A., Politz S.M., Daniels C.C., Tan L., and Drace K. Caenorhabditis elegans mutants resistant to attachment of Yersinia biofilms. Genetics 176 (2007) 221-230
21. De Arruda M.V., Colli W., and Zingales B. Terminal beta-d-galactofuranosyl epitopes recognized by antibodies that inhibit Trypanosoma cruzi internalization into mammalian cells. Eur. J. Biochem. 182 (1989) 413-421
22. de Lederkremer R.M., and Colli W. Galactofuranose-containing glycoconjugates in trypanosomatids. Glycobiology 5 (1995) 547-552
23. Dell A., Haslam S.M., Morris H.R., and Khoo K.H. Immunogenic glycoconjugates implicated in parasitic nematode diseases. Biochim. Biophys. Acta 1455 (1999) 353-362
24. Despommier D.D., Gold A.M., Buck S.W., Capo V., and Silberstein D. Trichinella spiralis: secreted antigen of the infective L1 larva localizes to the cytoplasm and nucleoplasm of infected host cells. Exp. Parasitol. 71 (1990) 27-38
25. Desvergnes S., Desvergnes V., Martin O.R., Itoh K., Liu H.W., and Py S. Stereoselective synthesis of beta-1-C-substituted 1,4-dideoxy-1,4-imino-d-galactitols and evaluation as UDP-galactopyranose mutase inhibitors. Bioorg. Med. Chem. 15 (2007) 6443-6449
26. Dykhuizen E.C., May J.F., Tongpenyai A., and Kiessling L.L. Inhibitors of UDP-galactopyranose mutase thwart mycobacterial growth. J. Am. Chem. Soc. 130 (2008) 6706-6707
27. El-Ganiny A.M., Sanders D.A., and Kaminskyj S.G. Aspergillus nidulans UDP-galactopyranose mutase, encoded by ugmA plays key roles in colony growth, hyphal morphogensis, and conidiation. Fungal Genet. Biol. 45 (2008) 1533-1542
28. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., and Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 (1998) 806-811
29. Ghavami A., Chen J.J., and Mario Pinto B. Synthesis of a novel class of sulfonium ions as potential inhibitors of UDP-galactopyranose mutase. Carbohydr. Res. 339 (2004) 401-407
30. Gravato-Nobre M.J., and Hodgkin J. The acyltransferase gene bus-1 exhibits conserved and specific expression in nematode rectal cells and reveals pathogen-induced cell swelling. Dev. Dyn. 237 (2008) 3762-3776
31. Gravato-Nobre M.J., Nicholas H.R., Nijland R., O'Rourke D., Whittington D.E., Yook K.J., and Hodgkin J. Multiple genes affect sensitivity of Caenorhabditis elegans to the bacterial pathogen Microbacterium nematophilum. Genetics 171 (2005) 1033-1045
32. Guerardel Y., Balanzino L., Maes E., Leroy Y., Coddeville B., Oriol R., and Strecker G. The nematode Caenorhabditis elegans synthesizes unusual O-linked glycans: identification of glucose-substituted mucin-type O-glycans and short chondroitin-like oligosaccharides. Biochem. J. 357 (2001) 167-182
33. Harnett W., and Harnett M.M. Modulation of the host immune system by phosphorylcholine-containing glycoproteins secreted by parasitic filarial nematodes. Biochim. Biophys. Acta 1539 (2001) 7-15
34. Hearn V.M., Griffiths B.L., and Gorin P.A. Structural analysis of water-soluble fractions obtained from Aspergillus fumigatus mycelium. Glycoconj. J. 6 (1989) 85-100
35. Hodgkin J., Kuwabara P.E., and Corneliussen B. A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans. Curr. Biol. 10 (2000) 1615-1618
36. Hoflich J., Berninsone P., Gobel C., Gravato-Nobre M.J., Libby B.J., Darby C., Politz S.M., Hodgkin J., Hirschberg C.B., and Baumeister R. Loss of srf-3-encoded nucleotide sugar transporter activity in Caenorhabditis elegans alters surface antigenicity and prevents bacterial adherence. J. Biol. Chem. 279 (2004) 30440-30448
37. Hwang H.Y., and Horvitz H.R. The SQV-1 UDP-glucuronic acid decarboxylase and the SQV-7 nucleotide-sugar transporter may act in the Golgi apparatus to affect Caenorhabditis elegans vulval morphogenesis and embryonic development. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 14218-14223
38. Ilg T., Etges R., Overath P., McConville M.J., Thomas-Oates J., Thomas J., Homans S.W., and Ferguson M.A. Structure of Leishmania mexicana lipophosphoglycan. J. Biol. Chem. 267 (1992) 6834-6840
39. Itoh K., Huang Z., and Liu H.W. Synthesis and analysis of substrate analogues for UDP-galactopyranose mutase: implication for an oxocarbenium ion intermediate in the catalytic mechanism. Org. Lett. 9 (2007) 879-882
40. James P.G., and Cherniak R. Galactoxylomannans of Cryptococcus neoformans. Infect. Immun. 60 (1992) 1084-1088
41. Johnston W.L., Krizus A., and Dennis J.W. The eggshell is required for meiotic fidelity, polar-body extrusion and polarization of the C. elegans embryo. BMC Biol. 4 (2006) 35
42. Johnstone I.L., and Barry J.D. Temporal reiteration of a precise gene expression pattern during nematode development. EMBO J. 15 (1996) 3633-3639
43. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., and Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421 (2003) 231-237
44. Khoo K.H., Maizels R.M., Page A.P., Taylor G.W., Rendell N.B., and Dell A. Characterization of nematode glycoproteins: the major O-glycans of Toxocara excretory-secretory antigens are O-methylated trisaccharides. Glycobiology 1 (1991) 163-171
45. Kleczka B., Lamerz A.C., van Zandbergen G., Wenzel A., Gerardy-Schahn R., Wiese M., and Routier F.H. Targeted gene deletion of Leishmania major UDP-galactopyranose mutase leads to attenuated virulence. J. Biol. Chem. 282 (2007) 10498-10505
46. Koplin R., Brisson J.R., and Whitfield C. UDP-galactofuranose precursor required for formation of the lipopolysaccharide O antigen of Klebsiella pneumoniae serotype O1 is synthesized by the product of the rfbDKPO1 gene. J. Biol. Chem. 272 (1997) 4121-4128
47. Kremer L., Dover L.G., Morehouse C., Hitchin P., Everett M., Morris H.R., Dell A., Brennan P.J., McNeil M.R., Flaherty C., Duncan K., and Besra G.S. Galactan biosynthesis in Mycobacterium tuberculosis. Identification of a bifunctional UDP-galactofuranosyltransferase. J. Biol. Chem. 276 (2001) 26430-26440
48. Link C.D., Silverman M.A., Breen M., Watt K.E., and Dames S.A. Characterization of Caenorhabditis elegans lectin-binding mutants. Genetics 131 (1992) 867-881
49. Maduro M., and Pilgrim D. Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141 (1995) 977-988
50. Maizels R.M., Kennedy M.W., Meghji M., Robertson B.D., and Smith H.V. Shared carbohydrate epitopes on distinct surface and secreted antigens of the parasitic nematode Toxocara canis. J. Immunol. 139 (1987) 207-214
51. McConville M.J., Homans S.W., Thomas-Oates J.E., Dell A., and Bacic A. Structures of the glycoinositolphospholipids from Leishmania major. A family of novel galactofuranose-containing glycolipids. J. Biol. Chem. 265 (1990) 7385-7394
52. McVay C.S., Tsung A., and Appleton J. Participation of parasite surface glycoproteins in antibody-mediated protection of epithelial cells against Trichinella spiralis. Infect. Immun. 66 (1998) 1941-1945
53. Mello C.C., Kramer J.M., Stinchcomb D., and Ambros V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10 (1991) 3959-3970
54. Mikusova K., Belanova M., Kordulakova J., Honda K., McNeil M.R., Mahapatra S., Crick D.C., and Brennan P.J. Identification of a novel galactosyl transferase involved in biosynthesis of the mycobacterial cell wall. J. Bacteriol. 188 (2006) 6592-6598
55. Moribe H., Yochem J., Yamada H., Tabuse Y., Fujimoto T., and Mekada E. Tetraspanin protein (TSP-15) is required for epidermal integrity in Caenorhabditis elegans. J. Cell. Sci. 117 (2004) 5209-5220
56. Nassau P.M., Martin S.L., Brown R.E., Weston A., Monsey D., McNeil M.R., and Duncan K. Galactofuranose biosynthesis in Escherichia coli K-12: identification and cloning of UDP-galactopyranose mutase. J. Bacteriol. 178 (1996) 1047-1052
57. Nielsen K., and Heitman J. Sex and virulence of human pathogenic fungi. Adv. Genet. 57 (2007) 143-173
58. Novelli J., Page A.P., and Hodgkin J. The C terminus of collagen SQT-3 has complex and essential functions in nematode collagen assembly. Genetics 172 (2006) 2253-2267
59. Page, A.P., and Johnstone, I.L., (2007). The cuticle. In "Wormbook doi/10.1895/wormbook.1.7.1, http://www.wormbook.org." (T. C. e. r. community, Ed.
60. Page A.P., Rudin W., Fluri E., Blaxter M.L., and Maizels R.M. Toxocara canis: a labile antigenic surface coat overlying the epicuticle of infective larvae. Exp. Parasitol. 75 (1992) 72-86
61. Pan F., Jackson M., Ma Y., and McNeil M. Cell wall core galactofuran synthesis is essential for growth of mycobacteria. J. Bacteriol. 183 (2001) 3991-3998
62. Partridge F.A., Tearle A.W., Gravato-Nobre M.J., Schafer W.R., and Hodgkin J. The C. elegans glycosyltransferase BUS-8 has two distinct and essential roles in epidermal morphogenesis. Dev. Biol. 317 (2008) 549-559
63. Pedersen L.L., and Turco S.J. Galactofuranose metabolism: a potential target for antimicrobial chemotherapy. Cell. Mol. Life Sci. 60 (2003) 259-266
64. Pemberton A.D., Knight P.A., Gamble J., Colledge W.H., Lee J.K., Pierce M., and Miller H.R. Innate BALB/c enteric epithelial responses to Trichinella spiralis: inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. J. Immunol. 173 (2004) 1894-1901
65. Plackett P., and Buttery S.H. A galactofuranose disaccharide from the galactan of Mycoplasma mycoides. Biochem. J. 90 (1964) 201-205
66. Poirot O., O'Toole E., and Notredame C. Tcoffee@igs: a web server for computing, evaluating and combining multiple sequence alignments. Nucleic Acids Res. 31 (2003) 3503-3506
67. Previato J.O., Gorin P.A., Mazurek M., Xavier M.T., Fournet B., Wieruszesk J.M., and Mendonca-Previato L. Primary structure of the oligosaccharide chain of lipopeptidophosphoglycan of epimastigote forms of Trypanosoma cruzi. J. Biol. Chem. 265 (1990) 2518-2526
68. Rabina J., Maki M., Savilahti E.M., Jarvinen N., Penttila L., and Renkonen R. Analysis of nucleotide sugars from cell lysates by ion-pair solid-phase extraction and reversed-phase high-performance liquid chromatography. Glycoconj. J. 18 (2001) 799-805
69. Rual J.F., Ceron J., Koreth J., Hao T., Nicot A.S., Hirozane-Kishikawa T., Vandenhaute J., Orkin S.H., Hill D.E., van den Heuvel S., and Vidal M. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 14 (2004) 2162-2168
70. Sambrook J., Fritsch E.F., and Maniatis T. Molecular cloning. A laboratory manual. Second edition (1989), Cold Spring harbor laboratory press
71. Samuelson A.V., Carr C.E., and Ruvkun G. Gene activities that mediate increased life span of C. elegans insulin-like signaling mutants. Genes Dev. 21 (2007) 2976-2994
72. Sanders D.A., Staines A.G., McMahon S.A., McNeil M.R., Whitfield C., and Naismith J.H. UDP-galactopyranose mutase has a novel structure and mechanism. Nat. Struct. Biol. 8 (2001) 858-863
73. Sarvas M., and Nikaido H. Biosynthesis of T1 antigen in Salmonella: origin of d-galactofuranose and d-ribofuranose residues. J. Bacteriol. 105 (1971) 1063-1072
74. Schabussova I., Amer H., van Die I., Kosma P., and Maizels R.M. O-methylated glycans from Toxocara are specific targets for antibody binding in human and animal infections. Int. J. Parasitol. 37 (2007) 97-109
75. Scherman M.S., Winans K.A., Stern R.J., Jones V., Bertozzi C.R., and McNeil M.R. Drug targeting Mycobacterium tuberculosis cell wall synthesis: development of a microtiter plate-based screen for UDP-galactopyranose mutase and identification of an inhibitor from a uridine-based library. Antimicrob. Agents Chemother. 47 (2003) 378-382
76. Schmalhorst P.S., Krappmann S., Vervecken W., Rohde M., Muller M., Braus G.H., Contreras R., Braun A., Bakker H., and Routier F.H. Contribution of galactofuranose to the virulence of the opportunistic pathogen Aspergillus fumigatus. Eukaryotic Cell 7 (2008) 1268-1277
77. Sharon E., Spiegel Y., Salomon R., and Curtis R.H. Characterization of Meloidogyne javanica surface coat with antibodies and their effect on nematode behaviour. Parasitology 125 (2002) 177-185
78. Silverman M.A., Blaxter M.L., and Link C.D. Biochemical analysis of Caenorhabditis elegans surface mutants. J. Nematol. 29 (1997) 296-305
79. Simmer F., Moorman C., van der Linden A.M., Kuijk E., van den Berghe P.V., Kamath R.S., Fraser A.G., Ahringer J., and Plasterk R.H. Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol. 1 (2003) E12
80. Singh R.N., and Sulston J.E. Some observations on molting in C. elegans. Nematologica (1978) 24
81. Solomon A., Bandhakavi S., Jabbar S., Shah R., Beitel G.J., and Morimoto R.I. Caenorhabditis elegans OSR-1 regulates behavioral and physiological responses to hyperosmotic environments. Genetics 167 (2004) 161-170
82. Soltero-Higgin M., Carlson E.E., Phillips J.H., and Kiessling L.L. Identification of inhibitors for UDP-galactopyranose mutase. J. Am. Chem. Soc. 126 (2004) 10532-10533
83. Spath G.F., Garraway L.A., Turco S.J., and Beverley S.M. The role(s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 9536-9541
84. Stevenson G., Neal B., Liu D., Hobbs M., Packer N.H., Batley M., Redmond J.W., Lindquist L., and Reeves P. Structure of the O antigen of Escherichia coli K-12 and the sequence of its rfb gene cluster. J. Bacteriol. 176 (1994) 4144-4156
85. Sulston J.E., and Hodgkin J.A. Methods. In: Press C.S.H.L. (Ed). The nematode Caenorhabditis elegans (1988) 587-606
86. Thacker C., Peters K., Srayko M., and Rose A.M. The bli-4 locus of Caenorhabditis elegans encodes structurally distinct kex2/subtilisin-like endoproteases essential for early development and adult morphology. Genes Dev. 9 (1995) 956-971
87. Trejo A.G., Chittenden G.J., Buchanan J.G., and Baddiley J. Uridine diphosphate alpha-d-galactofuranose, an intermediate in the biosynthesis of galactofuranosyl residues. Biochem. J. 117 (1970) 637-639
88. Tsuji S., Uehori J., Matsumoto M., Suzuki Y., Matsuhisa A., Toyoshima K., and Seya T. Human intelectin is a novel soluble lectin that recognizes galactofuranose in carbohydrate chains of bacterial cell wall. J. Biol. Chem. 276 (2001) 23456-23463
89. Turco S.J., Orlandi Jr. P.A., Homans S.W., Ferguson M.A., Dwek R.A., and Rademacher T.W. Structure of the phosphosaccharide-inositol core of the Leishmania donovani lipophosphoglycan. J. Biol. Chem. 264 (1989) 6711-6715
90. Turnock D.C., and Ferguson M.A. The sugar nucleotide pools of Trypanosoma brucei, Trypanosoma cruzi and Leishmania major. Eukaryot Cell 6 (2007) 1450-1463
91. Varki A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3 (1993) 97-130
92. Veerapen N., Yuan Y., Sanders D.A., and Pinto B.M. Synthesis of novel ammonium and selenonium ions and their evaluation as inhibitors of UDP-galactopyranose mutase. Carbohydr. Res. 339 (2004) 2205-2217
93. Voehringer D., Stanley S.A., Cox J.S., Completo G.C., Lowary T.L., and Locksley R.M. Nippostrongylus brasiliensis: identification of intelectin-1 and -2 as Stat6-dependent genes expressed in lung and intestine during infection. Exp. Parasitol. 116 (2007) 458-466
94. Wallis G.L., Hemming F.W., and Peberdy J.F. Beta-galactofuranoside glycoconjugates on conidia and conidiophores of Aspergillus niger. FEMS Microbiol. Lett. 201 (2001) 21-27
95. Weston A., Stern R.J., Lee R.E., Nassau P.M., Monsey D., Martin S.L., Scherman M.S., Besra G.S., Duncan K., and McNeil M.R. Biosynthetic origin of mycobacterial cell wall galactofuranosyl residues. Tuber. Lung Dis. 78 (1997) 123-131
96. Wing C., Errey J.C., Mukhopadhyay B., Blanchard J.S., and Field R.A. Expression and initial characterization of WbbI, a putative d-Galf:alpha-d-Glc beta-1,6-galactofuranosyltransferase from Escherichia coli K-12. Org. Biomol. Chem. 4 (2006) 3945-3950
97. Winter A.D., and Page A.P. Prolyl 4-hydroxylase is an essential procollagen-modifying enzyme required for exoskeleton formation and the maintenance of body shape in the nematode Caenorhabditis elegans. Mol. Cell. Biol. 20 (2000) 4084-4093
98. Wisnewski N., McNeil M., Grieve R.B., and Wassom D.L. Characterization of novel fucosyl- and tyvelosyl-containing glycoconjugates from Trichinella spiralis muscle stage larvae. Mol. Biochem. Parasitol. 61 (1993) 25-35
99. Yochem J., Gu T., and Han M. A new marker for mosaic analysis in Caenorhabditis elegans indicates a fusion between hyp6 and hyp7, two major components of the hypodermis. Genetics 149 (1998) 1323-1334
100. Yook K., and Hodgkin J. Mos1 mutagenesis reveals a diversity of mechanisms affecting response of Caenorhabditis elegans to the bacterial pathogen Microbacterium nematophilum. Genetics 175 (2007) 681-697
101. Zhang K., Barron T., Turco S.J., and Beverley S.M. The LPG1 gene family of Leishmania major. Mol. Biochem. Parasitol. 136 (2004) 11-23