Evidence for a sialic acid salvaging pathway in lepidopteran insect cells

Glycobiology

Volumn 13, Issue 6, 2003, Pages 487-495

  Hollister, Jason ^a   Conradt, Harald ^b   Jarvis, Donald L ^a  

^a UNIVERSITY OF WYOMING   (United States)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Baculovirus expression system; Glycoprotein biosynthesis; Insect cells; Sialic acids; Sialylation

Indexed keywords

ASIALOFETUIN; CYTIDINE PHOSPHATE; FETUIN; GLYCAN DERIVATIVE; GLYCOPROTEIN; MANNOSAMINE; N ACETYLNEURAMINIC ACID; RECOMBINANT PROTEIN; SIALIC ACID; SIALOGLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CELL LINE; CONTROLLED STUDY; DIALYSIS MEMBRANE; INSECT CELL; ISOLATION PROCEDURE; LEPIDOPTERA; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; SIALYLATION; TRANSGENIC ANIMAL;

ANIMALS; BACULOVIRIDAE; BIOLOGICAL FACTORS; CELL LINE, TRANSFORMED; CULTURE MEDIA, SERUM-FREE; LEPIDOPTERA; POLYSACCHARIDES; SERUM; SIALIC ACIDS; SIALOGLYCOPROTEINS;

ANIMALIA; ARACHNIDA; BOVINAE; HEXAPODA; INSECTA; LEPIDOPTERA; MAMMALIA; UNIDENTIFIED BACULOVIRUS;

EID: 0037567649     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/cwg053     Document Type: Article

References (45)

1. Altmann, F., Staudacher, E., Wilson, I.B., and Marz, L. (1999) Insect cells as hosts for the expression of recombinant glycoproteins. Glycoconj. J., 16, 109-123.
2. Angata, T. and Varki, A. (2000) Cloning, characterization, and phylogenetic analysis of siglec-9, a new member of the CD33-related group of siglecs. Evidence for co-evolution with sialic acid synthesis pathways. J. Biol. Chem., 275, 22127-22135.
3. Aumiller, J.J. and Jarvis, D.L. (2002) Expression and functional characterization of a nucleotide sugar transporter from Drosophila melanogaster: relevance to protein glycosylation in insect cell expression systems. Prot. Expr. Purif., 26, 438-448.
4. Aumiller, J.J., Hollister, J.R., and Jarvis, D.L. (2003) A transgenic insect cell line engineered to produce CMP-sialic acid and sialylated glycoproteins. Glycobiology, 13, 497-507.
5. Butters, T.D., Hughes, R.C., and Vischer, P. (1981) Steps in the biosynthesis of mosquito cell membrane glycoproteins and the effects of tunicamycin. Biochim. Biophys. Acta, 640, 672-686.
6. Chigorno, V., Tettamanti, G., and Sonnino, S. (1996) Metabolic processing of gangliosides by normal and Salla human fibroblasts in culture. A study performed by administering radioactive GM3 ganglioside. J. Biol. Chem., 271, 21738-21744.
7. Comb, D.G. (1966) The sialic acids. J. Biol. Chem., 241, 5637-5642.
8. Effertz, K., Hinderlich, S., and Reutter, W. (1999) Selective loss of either the epimerase or kinase activity of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase due to site-directed mutagenesis based on sequence alignments. J. Biol. Chem., 274, 28771-28778.
9. Ferraz, C., Vidal, S., Brun, C., Bucheton, A., and Demaille, J.G. (1999) Sequencing the distal x chromosome of Drosophila melanogaster. Genbank Accession Number AL023874.
10. Ferwerda, W., Blok, C.M., and Heijlman, J. (1981) Turnover of free sialic acid, CMP-sialic acid, and bound sialic acid in rat brain. J. Neurochem., 36, 1492-1499.
11. Ghosh, S. and Roseman, S. (1961) Enzymatic phosphorylation of N-acetyl-D-mannosamine. Proc. Natl Acad. Sci. USA, 47, 955-958.
12. Hardy, M.R. and Townsend, R.R. (1988) Separation of positional isomers of oligosaccharides and glycopeptides by high-performance anion-exchange chromatography with pulsed amperometric detection. Proc. Natl Acad. Sci. USA, 85, 3289-3293.
13. Hermentin, P., Witzel, R., Doenges, R., Bauer, R., Haupt, H., Patel, T., Parekh, R.B., and Brazel, D. (1992) The mapping by high-pH anion-exchange chromatography with pulsed amperometric detection and capillary electrophoresis of the carbohydrate moieties of human plasma alpha 1-acid glycoprotein. Anal. Biochem., 206, 419-429.
14. Hollister, J. and Jarvis, D.L. (2001) Engineering lepidopteran insect cells for sialoglycoprotein production by genetic transformation with mammalian β1,4-galactosyltransferase and alpha 2,6-sialyltransferase genes. Glycobiology, 11, 1-9.
15. Hollister, J.R., Shaper, J.H., and Jarvis, D.L. (1998) Stable expression of mammalian beta 1,4-galactosyltransferase extends the N-glycosylation pathway in insect cells. Glycobiology, 8, 473-480.
16. Hollister, J.R., Grabenhorst, E., Nimtz, M., Conradt, H.O., and Jarvis, D.L. (2002) Engineering the protein N-glycosylation pathway in insect cells for production of biantennary, complex N-glycans. Biochemistry, 41, 15093-15104.
17. Hooker, A.D., Green, N.H., Baines, A.J., Bull, A.T., Jenkins, N., Strange, P.G., and James, D.C. (1999) Constraints on the transport and glycosylation of recombinant IFN-gamma in Chinese hamster ovary and insect cells. Biotech. Bioengr., 63, 559-572.
18. Jarvis, D.L. (1993) Continuous foreign gene expression in stably-transformed insect cells. In: Goosen, M.F.A., Daugulis, A., and Faulkner, P. (Eds), Insect cell culture engineering. Marcel Dekker, New York, pp. 193-217.
19. Jarvis, D.L. (1997) Baculovirus expression vectors. In: Miller, L. K. (Ed), The baculoviruses. Plenum Press, New York, pp. 389-431.
20. Jarvis, D.L. and Finn, E.E. (1995) Biochemical analysis of the N-glycosylation pathway in baculovirus-infected lepidopteran insect cells. Virology, 212, 500-511.
21. Jarvis, D.L. and Finn, E.E. (1996) Modifying the insect cell N-glycosylation pathway with immediate early baculovirus expression vectors. Nature/Biotechnol., 14, 1288-1292.
22. Jarvis, D.L., Howe, D., and Aumiller, J.J. (2001) Novel baculovirus expression vectors that provide sialylation of recombinant glycoproteins in lepidopteran insect cells. J. Virol., 75, 6223-6227.
23. Kawar, Z., Romero, P.A., Herscovics, A., and Jarvis, D.L. (2000) N-glycan processing by a lepidopteran insect alpha 1,2-mannosidase. Glycobiology, 10, 347-355.
24. Kean, E.L. (1970) Nuclear cytidine 5′-monophosphosialic acid synthetase. J. Biol. Chem., 245, 2301-2308.
25. Kim, K., Lawrence, S.M., Park, J., Pitts, L., Vann, W.F., Betenbaugh, M.J., and Palter, K.B. (2002) Expression of a functional Drosophila melanogaster N-acetylneuraminic acid (Neu5Ac) phosphate synthase gene: evidence for endogenous sialic acid biosynthetic ability in insects. Glycobiology, 12, 73-83.
26. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
27. Lawrence, S.M., Huddleston, K.A., Pitts, L.R., Nguyen, N., Lee, Y.C., Vann, W.F., Coleman, T.A., and Betenbaugh, M.J. (2000) Cloning and expression of the human N-acetylneuraminic acid phosphate synthase gene with 2-keto-3-deoxy-D-glycero-D-galacto-nononic acid biosynthetic ability. J. Biol. Chem., 275, 17869-17877.
28. Licari, P.J., Jarvis, D.L., and Bailey, J.E. (1993) Insect cell hosts for baculovirus expression vectors contain endogenous exoglycosidase activity. Biotech. Progr., 9, 146-152.
29. Luckow, V.L. and Summers, M.D. (1988) Trends in the development of baculovirus expression vectors. Bio/Technology, 6, 47-55.
30. Marchal, I., Jarvis, D.L., Cacan, R., and Verbert, A. (2001) Glycoproteins from insect cells: sialylated or not? Biol. Chem., 382, 151-159.
31. Marz, L., Altmann, F., Staudacher, E., and Kubelka, V. (1995) Protein glycosylation in insects. In: Montreuil, J., Vliegenthart, J.F.G., and Schachter, H. (eds), Glycoproteins, vol. 29a. Elsevier, Amsterdam, pp. 543-563.
32. Mendla, K., Baumkotter, J., Rosenau, C., Ulrich-Bott, B., and Cantz, M. (1988) Defective lysosomal release of glycoprotein-derived sialic acid in fibroblasts from patients with sialic acid storage disease. Biochem. J., 250, 261-267.
33. O'Reilly, D.R., Miller, L.K., and Luckow, V.A. (1992) Baculovirus expression vectors. Freeman, New York.
34. Packer, N.H., Lawson, M.A., Jardine, D.R., and Redmond, J.W. (1998) A general approach to desalting oligosaccharides released from glycoproteins. Glycoconj. J., 15, 737-747.
35. Pfeifer, T.A. (1998) Expression of heterologous proteins in stable insect cell culture. Curr. Opin. Biotech., 9, 518-521.
36. Roseman, S., Jourdian, G.W., Walson, D., and Rood, R. (1961) Enzymatic synthesis of sialic acid-9-phosphate. Proc. Natl Acad. Sci. USA, 47, 958-961.
37. Schauer, R. and Corfield, A.P. (1982) Metabolism of sialic acids. In: Schauer, R. (ed), Sialic acids. Chemistry, metabolism and function, vol. 10. Springer-Verlag, Wien-New York, pp. 195-262.
38. Segawa, H., Kawakita, M., and Ishida, N. (2002) Human and Drosophila UDP-galactose transporters transport UDP-N-acetylgalactosamine in addition to UDP-galactose. Eur. J. Biochem., 269, 128-138.
39. Seo, N.S., Hollister, J.R., and Jarvis, D.L. (2001) Mammalian glycosyltransferase expression allows sialoglycoprotein production by baculovirus-infected insect cells. Prot. Expr. Purif., 22, 234-241.
40. Stollar, V., Stollar, B.D., Koo, R., Harrap, K.A., and Schlesinger, R.W. (1976) Sialic acid contents of sindbis virus from vertebrate and mosquito cells. Equivalence of biological and immunological viral properties. Virology, 69, 104-115.
41. Summers, M.D. and Smith, G.E. (1987) A manual of methods for baculovirus vectors and insect cell culture procedures. TX Ag. Expt. Stn. Bull. no. 1555.
42. Tomiya, N., Ailor, E., Lawrence, S.M., Betenbaugh, M.J., and Lee, Y.C. (2001) Determination of nucleotides and sugar nucleotides involved in protein glycosylation by high-performance anion-exchange chromatography: sugar nucleotide contents in cultured insect cells and mammalian cells. Anal. Biochem., 293, 129-137.
43. Warren, L. and Felsenfeld, H. (1961) The biosynthesis of N-acetylneuraminic acid. Biochem. Biophys. Res. Commun., 4, 232-253.
44. Watson, D.R., Jourdian, G.W., and Roseman, S. (1966) Sialic acid 9-phosphate synthetase. J. Biol. Chem., 241, 5627-5636.
45. Weinstein, J., Lee, E.U., McEntee, K., Lai, P.-H., and Paulson, J.C. (1987) Primary structure of β-galactoside alpha 2,6-sialyltransferase. Conversion of membrane-bound enzyme to soluble forms by cleavage of the NH2-terminal signal anchor. J. Biol. Chem., 262, 17735-17743.