Enzyme catalysed production of sialylated human milk oligosaccharides and galactooligosaccharides by Trypanosoma cruzi trans-sialidase

New Biotechnology

Volumn 31, Issue 2, 2014, Pages 156-165

  Holck, Jesper ^a   Larsen, Dorte M ^a   Michalak, Malwina ^a   Li, Haiying ^b   Kjærulff, Louise ^a   Kirpekar, Finn ^b   Gotfredsen, Charlotte H ^a   Forssten, Sofia ^c   Ouwehand, Arthur C ^c   Mikkelsen, Jørn D ^a   Meyer, Anne S ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c DUPONT COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEINS; FEMALE; GLYCOPROTEINS; HUMANS; MILK, HUMAN; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; OLIGOSACCHARIDES; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; TRYPANOSOMA CRUZI;

EID: 84893741493     PISSN: 18716784     EISSN: 18764347     Source Type: Journal    
DOI: 10.1016/j.nbt.2013.11.006     Document Type: Article

References (50)

1. Kunz C., Rudloff S. Health promoting aspects of milk oligosaccharides. Int Dairy J 2006, 16:1341-1346.
2. Locascio R.G., Ninonuevo M.R., Freeman S.L., Sela D.A., Grimm R., Lebrilla C.B., et al. Glycoprofiling of bifidobacterial consumption of human milk oligosaccharides demonstrates strain specific, preferential consumption of small chain glycans secreted in early human lactation. J Agric Food Chem 2007, 55:8914-8919.
3. Marcobal A., Barboza M., Froehlich J.W., Block D.E., German J.B., Lebrilla C.B., et al. Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem 2010, 58:5334-5340.
4. Ruiz-Palacios G.M., Cervantes L.E., Ramos P., Chavez-Munguia B., Newburg D.S. Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 2003, 278:14112-14120.
5. Eiwegger T., Stahl B., Schmitt J., Boehm G., Gerstmayr M., Pichler J., et al. Human milk-derived oligosaccharides and plant-derived oligosaccharides stimulate cytokine production of cord blood T-cells in vitro. Pediatr Res 2004, 56:536-540.
6. Kunz C., Rudloff S., Baier W. Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr 2000, 20:699-722.
7. Frantz DC. Prebiotic formulation to human useful modulating or stimulating growth of bifidobacteria in the human intestine, and as supplement to diet, comprises 2'-fucosyllactose, 3'-sialyllactose, and 6'-sialyllactose. US 2012/0208782-A1; 2012.
8. Idota T., Kawakami H., Murakami Y., Sugawara M. Inhibition of cholera-toxin by human-milk fractions and sialyllactose. Biosci Biotechnol Biochem 1995, 59:417-419.
9. Fuhrer A., Sprenger N., Kurakevich E., Borsig L., Chassard C., Hennet T. Milk sialyllactose influences colitis in mice through selective intestinal bacterial colonization. J Exp Med 2010, 207:2843-2854.
10. Wang B., McVeagh P., Petocz P., Brand-Miller J. Brain ganglioside and glycoprotein sialic acid in breastfed compared with formula-fed infants. Am J Clin Nutr 2003, 78:1024-1029.
11. Gopal P.K., Gill H.S. Oligosaccharides and glycoconjugates in bovine milk and colostrum. Br J Nutr 2000, 84:S69-S74.
12. Endo T., Koizumi S., Tabata K., Ozaki A. Large-scale production of CMP-NeuAc and sialylated oligosaccharides through bacterial coupling. Appl Microbiol Biotechnol 2000, 53:257-261.
13. Paris G., Ratier L., Amaya M.F., Nguyen T., Alzari P.M., Frasch A.C. A sialidase mutant displaying trans-sialidase activity. J Mol Biol 2005, 345:923-934.
14. Schauer R., Kamerling J.P. The chemistry and biology of trypanosomal trans-sialidases: virulence factors in Chagas disease and sleeping sickness. Chembiochem 2011, 12:2246-2264.
15. Cross G.A.M., Takle G.B. The surface trans-sialidase family of Trypanosoma cruzi. Annu Rev Microbiol 1993, 47:385-411.
16. Pelletier M, Barker WA, Hakes DJ, Zopf DA. Methods for producing sialyloligosaccharides in a dairy source. WO1999/08511; 1999.
17. Mcjarrow P, Garman J, Harvey S, Van Amelsfort A, Amelsfort AV. Production of sialyl-oligosaccharide and desialylated glycomacropeptide involves reacting sugar and glycomacropeptide in the presence of sialidase. WO2003/049547-A2; 2003.
18. Lee S.G., Shin D.H., Kim B.G. Production of sialyloligosaccharides by trans-sialidase catalysed reaction using fetuin as a sialic acid donor. Enzyme Microb Technol 2002, 31:742-746.
19. Campetella O.E., Uttaro A.D., Parodi A.J., Frasch A.C.C. A recombinant Trypanosoma cruzi trans-sialidase lacking the amino acid repeats retains the enzymatic activity. Mol Biochem Parasitol 1994, 64:337-340.
20. Fath S., Bauer A.P., Liss M., Spriestersbach A., Maertens B., Hahn P., et al. Multiparameter RNA and codon optimisation: a standardized tool to assess and enhance autologous mammalian gene expression. PLoS ONE 2011, 6:e17596.
21. Silva I.R., Larsen D.M., Meyer A.S., Mikkelsen J.D. Identification, expression, and characterisation of a novel bacterial RGI lyase enzyme for the production of bio-functional fibers. Enzyme Microb Technol 2011, 49:160-166.
22. Schrader S., Schauer R. Nonradioactive trans-sialidase screening assay. Methods Mol Biol 2006, 347:93-107.
23. Matsuno K., Suzuki S. Simple fluorimetric method for quantification of sialic acids in glycoproteins. Anal Biochem 2008, 375:53-59.
24. Saito T., Itoh T. Variations and distributions of o-glycosidically linked sugar chains in bovine kappa-casein. J Dairy Sci 1992, 75:1768-1774.
25. Holck J., Hjerno K., Lorentzen A., Vigsnaes L.K., Hemmingsen L., Licht T.R., et al. Tailored enzymatic production of oligosaccharides from sugar beet pectin and evidence of differential effects of a single DP chain length difference on human faecal microbiota composition after in vitro fermentation. Process Biochem 2011, 46:1039-1049.
26. Mäkeläinen H., Saarinen M., Stowell J., Rautonen N., Ouwehand A. Xylo-oligosaccharides and lactitol promote the growth of Bifidobacterium lactis and Lactobacillus species in pure cultures. Benef Microbes 2010, 1:139-148.
27. Koliwer-Brandl H., Gbem T.T., Waespy M., Reichert O., Mandel P., Drebitz P., et al. Biochemical characterisation of trans-sialidase TS1 variants from Trypanosoma congolense. BMC Biochem 2011, 12:39.
28. Schenkman S., Decarvalho L., Nussenzweig V. Trypanosoma cruzi trans-sialidase and neuraminidase activities can be mediated by the same enzymes. J Exp Med 1992, 175:567-575.
29. Ribeirao M., Pereira-Chioccola V., Eichinger D., Rodrigues M., Schenkman S. Temperature differences for trans-glycosylation and hydrolysis reaction reveal an acceptor binding site in the catalytic mechanism of Trypanosoma cruzi trans-sialidase. Glycobiology 1997, 7:1237-1246.
30. Buschiazzo A., Tavares G.A., Campetella O., Spinelli S., Cremona M.L., Paris G., et al. Structural basis of sialyltransferase activity in trypanosomal sialidases. EMBO J 2000, 19:16-24.
31. Ninonuevo M.R., Park Y., Yin H., Zhang J., Ward R.E., Clowers B.H., et al. A strategy for annotating the human milk glycome. J Agric Food Chem 2006, 54:7471-7480.
32. Ruhaak L.R., Deelder A.M., Wuhrer M. Oligosaccharide analysis by graphitized carbon liquid chromatography-mass spectrometry. Anal Bioanal Chem 2009, 394:163-174.
33. Sabesan S., Paulson J.C. Combined chemical and enzymatic-synthesis of sialyloligosaccharides and characterisation by 500-Mhz H-1 and C-13 NMR-spectroscopy. J Am Chem Soc 1986, 108:2068-2080.
34. Lerner L., Bax A. Application of new, high-sensitivity, H-1-C-13-NMR spectral techniques to the study of oligosaccharides. Carbohydr Res 1987, 166:35-46.
35. Platzer N., Davoust D., Lhermitte M., Bauvy C., Meyer D.M., Derappe C. Structural analysis of 5 lactose-containing oligosaccharides by improved, high-resolution, two-dimensional H-1-NMR spectroscopy. Carbohydr Res 1989, 191:191-207.
36. Kunz C., Rudloff S. Biological functions of oligosaccharides in human-milk. Acta Paediatr 1993, 82:903-912.
37. Agusti R., Giogi M.E., Mendoz V.M., Gallo-Rodriguez C., de Lederkremer R.M. Comparative rates of sialylation by recombinant trans-sialidase and inhibitor properties of synthetic oligosaccharides from Trypanosoma cruzi mucins-containing galactofuranose and galactopyranose. Bioorg Med Chem 2007, 15:2611-2616.
38. Agusti R., Paris G., Ratier L., Frasch A.C.C., de Lederkremer R.M. Lactose derivatives are inhibitors of Trypanosoma cruzi trans-sialidase activity toward conventional substrates in vitro and in vivo. Glycobiol 2004, 14:659-670.
39. Harrison J.A., Kartha K.P.R., Fournier E.J.L., Lowary T.L., Malet C., Nilsson U.J., et al. Probing the acceptor substrate binding site of Trypanosoma cruzi trans-sialidase with systematically modified substrates and glycoside libraries. Org Biomol Chem 2011, 9:1653-1660.
40. de Lederkremer R.M., Agusti R. Glycobiology of Trypanosoma cruzi. Adv Carb Chem Biochem 2009, 62:311-365.
41. Vandekerckove F., Schenkman S., Decarvalho L., Tomlinson S., Kiso M., Yoshida M., et al. Substrate-specificity of the Trypanosoma cruzi trans-sialidase. Glycobiology 1992, 2:541-548.
42. Sela D.A., Chapman J., Adeuya A., Kim J.H., Chen F., Whitehead T.R., et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilisation within the infant microbiome. Proc Natl Acad Sci U S A 2008, 105:18964-18969.
43. Kiyohara M., Tanigawa K., Chaiwangsri T., Katayama T., Ashida H., Yamamoto K. An exo-α-sialidase from bifidobacteria involved in the degradation of sialyloligosaccharides in human milk and intestinal glycoconjugates. Glycobiology 2011, 21:437-447.
44. Ward R.E., Ninonuevo M., Mills D.A., Lebrilla C.B., German J.B. In vitro fermentability of human milk oligosaccharides by several strains of bifidobacteria. Mol Nutr Food Res 2007, 51:1398-1405.
45. Thomassen L.V., Vigsnaes L.K., Licht T.R., Mikkelsen J.D., Meyer A.S. Maximal release of highly bifidogenic soluble dietary fibers from industrial potato pulp by minimal enzymatic treatment. Appl Microbiol Biotechnol 2011, 90:873-884.
46. Walters D.M., Stirewalt V.L., Melville S.B. Cloning, sequence, and transcriptional regulation of the operon encoding a putative N-acetylmannosamine-6-phosphate epimerase (nanE) and sialic acid lyase (nanA) in Clostridium perfringens. J Bacteriol 1999, 181:4526-4532.
47. Schrader S., Tiralongo E., Paris G., Yoshino T., Schauer R. A nonradioactive 96-well plate assay for screening of trans-sialidase activity. Anal Biochem 2003, 322:139-147.
48. Sartor P.A., Agusti R., Leguizamon M.S., Campetella O., de Lederkremer R.M. Continuous nonradioactive method for screening trypanosomal trans-sialidase activity and its inhibitors. Glycobiology 2010, 20:982-990.
49. Singh S., Scigelova M., Hallberg M.L., Howarth O.W., Schenkman S., Crout D.H.G. Synthesis of sialyloligosaccharides using the trans-sialidase from Trypanosoma cruzi: novel branched and di-sialylated products from digalactoside acceptors. Chem Commun 2000, 101:3-4.
50. Scudder P., Doom J.P., Chenkova M., Manger I.D., Pereira M.E.S. Enzymatic characterisation of beta-d-galactoside alpha 2,3-trans-sialidase from Trypanosoma cruzi. J Biol Chem 1993, 268:9886-9891.