Sialyltransferases of marine bacteria efficiently utilize glycosphingolipid substrates

Glycobiology

Volumn 20, Issue 2, 2009, Pages 187-198

  Kushi, Yasunori ^a   Kamimiya, Hisashi ^a   Hiratsuka, Hiroko ^a   Nozaki, Hirofumi ^a   Fukui, Hiroshi ^a   Yanagida, Mayumi ^a   Hashimoto, Makoto ^b   Nakamura, Kimihide ^a   Watarai, Shinobu ^c   Kasama, Takeshi ^d   Kajiwara, Hitomi ^e   Yamamoto, Takeshi ^e  

^a OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c Osaka Prefecture University   (Japan)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^e Japan Tabacco Inc   (Japan)

Author keywords

Bacterial sialyltransferase; Gangliosides synthesis; Ii antigens; In vitro synthesis; Sialylparagloboside

Indexed keywords

GANGLIOSIDE; GLYCOSPHINGOLIPID; PARAGLOBOSIDE; SIALYLTRANSFERASE; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; ENZYME BINDING; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; INFLUENZA VIRUS A H3N2; KIDNEY CELL; LIPOGENESIS; MARINE BACTERIUM; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SIALYLATION; CHEMISTRY; ENZYMOLOGY; ISOLATION AND PURIFICATION; METABOLISM; PH; PHOTOBACTERIUM; SYNTHESIS; TEMPERATURE;

BACTERIA (MICROORGANISMS); INFLUENZA A VIRUS; MAMMALIA; SIA;

GANGLIOSIDES; HYDROGEN-ION CONCENTRATION; PHOTOBACTERIUM; RECOMBINANT PROTEINS; SIALYLTRANSFERASES; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 77649209941     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwp160     Document Type: Article

References (67)

1. Angata T, Varki A. 2002. Chemical diversity in the sialic acids and related α-keto acids: An evolutionary perspective. Chem Rev. 102:439-469.
2. Ariga T, Yu RK. 2005. Antiglycolipid antibodies in Guillain-Barré syndrome and related diseases: Review of clinical features and antibody specificities. J Neurosci Res. 80:1-17.
3. Aspinall GO, McDonald AG, Pang H, Kurjanczyk LA, Penner JL. 1994. Lipopolysaccharides of Campylobacter jejuni serotype O:19: Structures of core oligosaccharide regions from the serostrain and two bacterial isolates from patients with the Guillain-Barré syndrome. Biochemistry. 33:241-249.
4. Bardor M, Nguyen DH, Diaz S, Varki A. 2005. Mechanism of uptake and incorporation of the non-human sialic acid N-glycolylneuraminic acid into human cells. J Biol Chem. 280:4228-4237.
5. Becker A, Reith A, Napiwotzki J, Kadenbach B. 1996. A quantitative method of determining initial amounts of DNA by polymerase chain reactions cycle titration using digital imaging and a novel DNA stain. Anal Biochem. 237:204-207.
6. Bremer Schlessinger EG J, Hakomori S. 1986. Ganglioside-mediated modulation of cell growth. Specific effects of GM3 on tyrosine phosphorylation of the epidermal growth factor receptor. J Biol Chem. 261:2434-2440.
7. Chiu CPC, Watts AG, Lairson LL, Gilbert M, Lim D, Wakarchuk WW, Withers SG, Strynadka NCJ. 2004. Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog. Nat Struct Mol Biol. 11:163-170.
8. Ciucanu I, Kerek F. 1984. A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res. 131:209-217.
9. Connor RJ, Kawaoka Y, Webster RG, Paulson JC. 1994. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolate. Virology. 205:17-23.
10. Fox KL, Cox AD, Gilbert M, Wakarchuk WW, Li J, Makepeace K, Richards JC, Moxon ER, HoodDW. 2006. Identification of a bifunctional lipopolysaccharide sialyltransferase in Haemophilus influenzae. J Biol Chem. 281:40024-40032.
11. Francois C, Marshall RD, Neuberger A. 1962. Carbohydrates in protein: 4. The determination of mannose in hen's-egg albumin by radioisotope dilution. Biochem J. 83:335-341.
12. Gagneux P, Varki A. 1999. Evolutionary considerations in relating oligosaccharide diversity to biological function. Glycobiology. 9:747-755.
13. Gilbert M, Brisson J-R, Karwaski M-F, Michniewicz J, Cunningham A-M, Wu Y, Young NM, Wakarchuk WW. 2000. Biosynthesis of ganglioside mimics in Campylobacter jejuni OH4384. J Biol Chem. 275:3896-3906.
14. Gilbert M, Karwaski M-F, Bernatchez S, Young NM, Taboada E, Michniewicz J, Cunningham A-M, WakarchukWW. 2002. The genetic bases for the variation in the lipo-oligosaccharide of the mucosal pathogen, Campylobacter jejuni. J Biol Chem. 277:327-337.
15. Godschalk PCR, Kuijf ML, Li J, Michael F St, Ang CW, Jacobs BC, Karwaski M-F, Brochu D, Moterassed A, Endtz HP, et al. 2007. Structural characterization of Campylobacter jejuni lipooligosaccharide outer cores associated with Guillain-Barré and Miller Fisher syndromes. Infect Immun. 75:1245-1254.
16. Guerry P, Szymanski CM, Prendergast MM, Hickey TE, Ewing CP, Pattarini DL, Moran AP. 2002. Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect Immun. 70:787-793.
17. Hakomori S-I. 1984. Tumor-associated carbohydrate antigens. Annu Rev Immunol. 2:103-126.
18. Hakomori S-I. 2002. The glycosynapse. Proc Natl Acad Sci USA. 99:225-232.
19. Hakomori S, Kannagi R. 1983. Glycosphingolipids as tumor-associated and differentiation markers. J Natl Cancer Inst. 71:231-251.
20. Hamanaka Y, Hamanaka S, Shinagawa Y, Suzuki T, Inagaki F, Suzuki M, Suzuki A. 1994. Ganglioside antigen of DU-PAN-2 in a human pancreatic cancer. FEBS Lett. 353:48-52.
21. Hashimoto Y, Abe M, Kiuchi Y, Suzuki A, Yamakawa T. 1984. Genetically regulated expression of UDP-N-acetylgalactosamine:GM3 (NeuGc) N-acetylgalactosaminyltransferase [EC 2.4.1.92] activity in mouse liver. J Biochem. 95:1543-1549.
22. Ishikawa D, Taki T. 2000. Thin-layer chromatography blotting using polyvinylidene difluoride membrane (Far-Eastern Blotting) and its applications. Methods Enzymol. 312:145-157.
23. IUPAC-IUB Commission Biochemical Nomeclature (CBN). 1976. The nomenclature of lipids. Eur J Biochem. 79:11-21.
24. Kajihara Y, Akai S, Nakagawa T, Sato R, Ebata T, Kodama H, Sato K-I. 1999. Enzymatic synthesis of Kdn oligosaccarides by a bacterial α-(2→6)-sialyltransferase. Carbohydr Res. 315:137-141.
25. Kajihara Y, Yamamoto T, Nagae H, Nakashizuka M, Sakakibara T, Terada I. 1996. A novel α2, 6-sialyltransferase: Transfer of sialic acid to fucosyl and sialyl trisaccharides. J Org Chem. 61:8632-8635.
26. Kasahara K, Guo L, Nagai Y, Sanai Y. 1994. Enzymatic assay of glycosphingolipid sialyltransferase using reverse-phase thin-layer chromatography. Anal Biochem. 218:224-226.
27. Kushi Y, Shimizu M, Watanabe K, Kasama T, Watarai S, Ariga T, Handa S. 2001. Characterization of blood group ABO (H)-active gangliosides in type ABerythrocytes and structural analysis of type A-active ganglioside variants in type A human erythrocytes. Biochim Biophys Acta. 1525:58-69.
28. Kushi Y, Tsunoda A, Komatsuzaki K, Watanabe K, Kasama T, Handa S. 1995. Characterization of blood-group-ABO(H)-active glycosphingolipids in type-AB human erythrocytes. Eur J Biochem. 231:862-867.
29. Mansson J-E, Mo HQ, Egge H, Svennerholm L. 1986. Trisialosyllactosylceramide (GT3) is a ganglioside of human lung. FEBS Lett. 196:259-262.
30. Moran AP, Prendergast MM. 1998. Molecular mimicry in Campylobacter jejuni lipopolysaccharides and the development of Guillain-Barré syndrome. J Infect Dis. 178:1549-1551.
31. Nohara-Uchida K, Ohashi M. 1987. Isolation and characterization of major gangliosides from frog liver. J Biochem. 102:923-932.
32. Nojiri H, Stroud M, Hakomori S. 1991. A specific type of ganglioside as a modulator of insulin-dependent cell growth and insulin receptor tyrosine kinase activity. J Biol Chem. 266:4531-4537.
33. Nojiri H, Takaku F, Terui Y, Miura Y, Saito M. 1986. Gangliosides GM3: An acidic membrane component that increases during macrophage-like cell differentiation can induce monocytic differentiation of human myeloid and monocytoid leukemic cell lines HL-60 and U937. Proc Natl Acad Sci USA. 83:782-786.
34. Paulson JC. 1989. Glycopoteins: What are the sugar chains for? Trends Biochem Sci. 14:272-276.
35. Prendergast MM, Lastovica AJ, Moran AP. 1998. Lipopolysaccharides from Campylobacter jejuni O:41 strains associated with Guillain-Barré syndrome exhibit mimicry of GM1 ganglioside. Infect Immun. 66:3649-3655.
36. Salloway S, Mermel LA, Seamans M, Aspinall GO, Nam Shin JE, Kurjanczyk LA, Penner JL. 1996. Miller-Fisher syndrome associated with Campylobacter jejuni bearing lipopolysaccharide molecules that mimic human ganglioside GD3. Infect Immun. 64:2945-2949.
37. Schauer R. 1982. Chemistry, metabolism, and biological function of sialic acids.Advances Carbohydrate Chemistry and Biochemistry. Vol. 40. New York: Academic Press. p. 131-234.
38. Schauer R. 2004. Victor Ginsburg's influence on my research of the role of sialic acids in biological recognition. Arch Biochem Biophys. 426:132-141.
39. Skipski VP. 1975. Thin-layer chromatography of neutral glycosphingolipids. Methods Enzymol. 35:396-425.
40. Suzuki Y, Ito T, Suzuki T, Holland RE Jr, Chambers TM, Kiso M, Ishida H, Kawaoka Y. 2000. Sialic acid species as a determinant of the host range of influenza A viruses. J Virol. 74:11825-11831.
41. Suzuki Y, Nakao T, Ito T, Watanabe N, Toda Y, Xu G, Suzuki T, Kobayashi T, Kimura Y, Yamada A, et al. 1992 Structural determination of gangliosides that bind to influenza A, B, and C viruses by an improved binding assay: Strain-specific receptor epitopes in sialo-sugar chains. Virology. 189:121-131.
42. Svennerholm L. 1957. Quantitative estimation of sialic acids: II. A colorimetric resorcinol-hydrochloric acid method. Biochim Biophys Acta. 24:604- 611.
43. Svennerholm L. 1963. Chromatographic separation of human brain gangliosides. J Neurochem. 10:613-623.
44. Svennerholm L, Mandel P, Dreyfus H, Urban PF. (Eds) 1980. Structure and Functions of Gangliosides. New York: Plenum.
45. Takakura Y, Tsukamoto H, Yamamoto T. 2007. Molecular cloning, expression and properties of an α/β-galactoside α2, 3-sialyltransferase from Vibrio sp. JT-FAJ-16. J Biochem. 142:403-412.
46. Taki T, Ishikawa D, Handa S, Kasama T. 1995. Direct mass spectrometric analysis of glycosphingolipid transferred to a polyvinylidene difluoride membrane by thin-layer chromatography blotting. Anal Biochem. 225:24-27.
47. Tangvoranuntakul P, Gagneux P, Diaz S, Bardor M, Varki N, Varki A, Muchmore E. 2003. Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc Natl Acad Sci USA. 100:12045-12050.
48. Taniguchi N, Honke K, Fukuda M. 2002. Handbook of Glycosyltransferases and Related Genes. Tokyo: Springer-Verlag.
49. Totani K, Kubota T, Kuroda T, Murata T, Hidari KI-P, Suzuki T, Suzuki Y, Kobayashi K, Ashida H, Yamamoto K, et al. 2003. Chemoenzymatic synthesis and application of glycopolymers containing multivalent sialyloligosaccharides with a poly (L-glutamic acid) backbone for inhibition of infection by influenza viruses. Glycobiology. 13:315-326.
50. Tsuji S, Arita M, Nagai Y. 1983. GQ1b, a bioactive ganglioside that exhibits novel nerve growth factors (NGF)like activities in the two neuroblastoma cell lines. J Biochem. 94:303-306.
51. 2+ dependent protein kinase activity exists in the plasma membrane fraction of neuroblastoma cell line, GOTO. J Biochem. 97:969-972.
52. Tsukamoto H, Katakura Y, Yamamoto T. 2007. Purification, cloning and expression of an α/β-galactoside α-2, 3-sialyltransferase from a luminous marine bacteria, Photobacterium phosphoreum. J Biol Chem. 282:29794-29802.
53. Varki A. 1993. Biological roles of oligosaccharides: All of the theories are correct. Glycobiology. 3:97-130.
54. Varki A. 2001. N-Glycolylneuraminic acid deficiency in humans. Biochimie. 83:615-622.
55. Varki A. 2007. Glycan-based interactions involving vertebrate sialic-acidrecognizing proteins. Nature. 446:1023-1029.
56. Wakarchuk WW, Gilbert M, Martin A, Wu Y, Brisson J-R, Thibault P, Richard JC. 1998. Structures of an (-2, 6-sialylated lipooligosaccharide from Neisseria meningitidis immunotype L1. Eur J Biochem. 254:626-633.
57. Watarai S, Kushi Y, Shigeto R, Misawa N, Eishi Y, Handa S, Yasuda T. 1995. Production of monoclonal antibodies directed to Hanganutziu-Deicher active gangliosides, N-glycolylneuraminic acid containing gangliosides. J Biochem. 117:1062-1069.
58. Watarai S, Tana, Inoue K, Kushi Y, Isogai E, Yokota K, Naka K, Oguma K, Kodama H. 2001. Inhibition of Vero cell cytotoxic activity in Escherichia coli O157:H7 lysates by globotriaosylceramide, Gb3, from bovine milk. Biosci Biotechnol Biochem. 65:414-419.
59. Yamamoto T, Hamada Y, Ichikawa M, Kajiwara H, Mine T, Tsukamoto H, Takakura Y. 2007. A β-galactoside α2, 6-sialyltransferase produced by a marine bacterium, Photobacterium leiognathi JT-SHIZ-145, is active at pH 8. Glycobiology. 17:1167-1174.
60. Yamamoto T, Ichikawa M, Kakakura Y. 2008. Conserved amino acid sequences in the bacterial sialyltransferases belonging to glycosyltransferase family 80. Biochem Biophys Res Commun. 365:340-343.
61. Yamamoto T, Nakashizuka M, Kodama H, Kajihara Y, Terada I. 1996. Purification and characterization of a marine bacterial β-galactoside α2, 6-sialyltransferases from Photobacterium damsela JT0160. J Biochem. 120:104-110.
62. Yamamoto T, Nakashizuka M, Terada I. 1998. Cloning and expression of a marine bacterial β-galactoside α2, 6-sialyltransferase gene from Photobacterium damsela JT0160. J Biochem. 123:94-100.
63. Yamamoto T, Takakura Y, Tsukamoto H. 2006. Bacterial sialyltransferases. Trends Glycosci Glycotechnol. 18:253-265.
64. Yogeewaran G. 1983. Cell surface glycolipids and glycoproteins in malignant transformation. Adv Cancer Res. 38:289-350.
65. Yu RK, Usuki S, Ariga T. 2006. Ganglioside molecular mimicry and its pathological roles in Guillain-Barré syndrome and related diseases. Infect Immun. 74:6517-6527.
66. Yuki N. 2005. Carbohydrate mimicry:Anewparadigm of autoimmune diseases. Curr Opin Immunol. 17:577-582.
67. Yuki N, Handa S, Taki T, Kasama T, Takahashi M, Saito K, Miyatake T. 1992. Cross-reactive antigen between nervous tissue and a bacterium elicits Guillain-Barré syndrome:molecular mimicry between ganglioside GM1 and lipopolysaccharide from Penner's serotype 19 of Campylobacter jejuni. Biomed Res. 13:451-453.