Glycoconjugate Journal

, Volume 21, Issue 6, pp 343–360

Comparing N-glycan processing in mammalian cell lines to native and engineered lepidopteran insect cell lines

  • Noboru Tomiya
  • Someet Narang
  • Yuan C. Lee
  • Michael J. Betenbaugh


In the past decades, a large number of studies in mammalian cells have revealed that processing of glycoproteins is compartmentalized into several subcellular organelles that process N-glycans to generate complex-type oligosaccharides with terminal N-acetlyneuraminic acid. Recent studies also suggested that processing of N-glycans in insect cells appear to follow a similar initial pathway but diverge at subsequent processing steps. N-glycans from insect cell lines are not usually processed to terminally sialylated complex-type structures but are instead modified to paucimannosidic or oligomannose structures. These differences in processing between insect cells and mammalian cells are due to insufficient expression of multiple processing enzymes including glycosyltransferases responsible for generating complex-type structures and metabolic enzymes involved in generating appropriate sugar nucleotides. Recent genomics studies suggest that insects themselves may include many of these complex transferases and metabolic enzymes at certain developmental stages but expression is lost or limited in most lines derived for cell culture. In addition, insect cells include an N-acetylglucosaminidase that removes a terminal N-acetylglucosamine from the N-glycan. The innermost N-acetylglucosamine residue attached to asparagine residue is also modified with α(1,3)-linked fucose, a potential allergenic epitope, in some insect cells. In spite of these limitations in N-glycosylation, insect cells have been widely used to express various recombinant proteins with the baculovirus expression vector system, taking advantage of their safety, ease of use, and high productivity. Recently, genetic engineering techniques have been applied successfully to insect cells in order to enable them to produce glycoproteins which include complex-type N-glycans. Modifications to insect N-glycan processing include the expression of missing glycosyltransferases and inclusion of the metabolic enzymes responsible for generating the essential donor sugar nucleotide, CMP-N-acetylneuraminic acid, required for sialylation. Inhibition of N-acetylglucosaminidase has also been applied to alter N-glycan processing in insect cells. This review summarizes current knowledge on N-glycan processing in lepidopteran insect cell lines, and recent progress in glycoengineering lepidopteran insect cells to produce glycoproteins containing complex N-glycans. Published in 2004.

insect cell baculovirus glycosylation neuraminic acid glycoprotein recombinant DNA biotechnology metabolic engineering 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Kulakosky PC, Shuler ML, Wood HA, N-glycosylation of a baculovirus-expressed recombinant glycoprotein in three insect cell lines, In Vitro Cell Dev Biol Anim 34, 101-8 (1998).Google Scholar
  2. 2.
    Lopez M, Coddeville B, Langridge J, Plancke Y, Sautiere P, Chaabihi H, Chirat F, Harduin-Lepers A, Cerutti M, Verbert A, Delannoy P, Microheterogeneity of the oligosac-charides carried by the recombinant bovine lactoferrin expressed in Mamestra brassicae cells, Glycobiology 7, 635-51 (1997).PubMedGoogle Scholar
  3. 3.
    Voss T, Ergulen E, Ahorn H, Kubelka V, Sugiyama K, Maurer-Fogy I, Glossl J, Expression of human interferon omega 1 in Sf9 cells. No evidence for complex-type N-linked glycosylation or sialylation, Eur J Biochem 217, 913-9 (1993).PubMedCrossRefGoogle Scholar
  4. 4.
    Grabenhorst E, Hofer B, Nimtz M, Jager V, Conradt HS, Biosyn-thesis and secretion of human interleukin 2 glycoprotein vari-ants from baculovirus-infected Sf21 cells. Characterization of polypeptides and posttranslational modifications, Eur J Biochem 215, 189-97 (1993).PubMedCrossRefGoogle Scholar
  5. 5.
    Kubelka V, Altmann F, Kornfeld G, Marz L, Structures of the N-linked oligosaccharides of the membrane glycoproteins from three lepidopteran cell lines (Sf-21, IZD-Mb-0503, Bm-N), Arch Biochem Biophys 308, 148-57 (1994).PubMedCrossRefGoogle Scholar
  6. 6.
    Wagner R, Liedtke S, Kretzschmar E, Geyer H, Geyer R, Klenk HD, Elongation of the N-glycans of fowl plague virus hemag-glutinin expressed in Spodoptera frugiperda (Sf9) cells by coexpression of human ß1,2-N-acetylglucosaminyltransferase I, Glycobiology 6, 165-75 (1996).PubMedGoogle Scholar
  7. 7.
    Ogonah OW, Freedman RB, Jenkins N, Patel K, Rooney B, Isolation and characterization of an insect cell line able to perform complex N-linked glycosylation on recombinant proteins, Bio/Technol 14, 197-202 (1996).CrossRefGoogle Scholar
  8. 8.
    Kretzschmar E, Geyer R, Klenk HD, Baculovirus infection does not alter N-glycosylation in Spodoptera frugiperda cells, Biological Chemistry Hoppe-Seyler 375, 23-7 (1994).Google Scholar
  9. 9.
    Aeed PA, Elhammer AP, Glycosylation of recombinant prorenin in insect cells: The insect cell line Sf9 does not express the man-nose 6-phosphate recognition signal, Biochemistry 33, 8793-7 (1994).PubMedCrossRefGoogle Scholar
  10. 10.
    Manneberg M, Friedlein A, Kurth H, Lahm HW, Fountoulakis M, Structural analysis and localization of the carbohydrate moi-eties of a soluble human interferon gamma receptor produced in baculovirus-infected insect cells, Protein Science 3, 30-8 (1994).PubMedCrossRefGoogle Scholar
  11. 11.
    Hogeland KE, Jr, Deinzer ML, Mass spectrometric studies on the N-linked oligosaccharides of baculovirus-expressed mouse interleukin-3, Biological Mass Spectrometry 23, 218-24 (1994).PubMedCrossRefGoogle Scholar
  12. 12.
    James DC, Freedman RB, Hoare M, Ogonah OW, Rooney BC, Larionov OA, Dobrovolsky VN, Lagutin OV, Jenkins N, N-glycosylation of recombinant human interferon-gammaproduced in different animal expression systems, Biotechnology (NY) 13, 592-6 (1995).CrossRefGoogle Scholar
  13. 13.
    James DC, Goldman MH, Hoare M, Jenkins N, Oliver RW, Green BN, Freedman RB, Posttranslational processing of recombinant human interferon-gamma in animal expression systems, Protein Sci 5, 331-40 (1996).PubMedGoogle Scholar
  14. 14.
    Kulakosky PC, Hughes PR, Wood HA, N-Linked glycosylation of a baculovirus-expressed recombinant glycoprotein in insect larvae and tissue culture cells, Glycobiology 8, 741-5 (1998).PubMedCrossRefGoogle Scholar
  15. 15.
    Kisielow M, Kleiner S, Nagasawa M, Faisal A, Nagamine Y, Isoform-specific knockdown and expression of adaptor protein ShcA using small interfering RNA, Biochem J 363, 1-5 (2002).PubMedCrossRefGoogle Scholar
  16. 16.
    Hsu TA, Takahashi N, Tsukamoto Y, Kato K, Shimada I, Masuda K, Whiteley EM, Fan JQ, Lee YC, Betenbaugh MJ, Differential N-glycan patterns of secreted and intracellular IgG produced in Trichoplusia ni cells, J Biol Chem 272, 9062-70 (1997).PubMedCrossRefGoogle Scholar
  17. 17.
    Choi O, Tomiya N, Kim JH, Slavicek JM, Betenbaugh MJ, Lee YC, N-glycan structures of human transferrin produced by Lymantria dispar (gypsy moth) cells using the LdMNPV expression system, Glycobiology 13, 539-48 (2003).PubMedCrossRefGoogle Scholar
  18. 18.
    Marz L, Altmann F, Staudacher E, Kubelka V, Protein glycosylation in insects. In Glycoproteins,Vol. 29a, edited by Montreuil J, Vliegenthart JFG, Schachter H (Elsevier, Amsterdam, 1995), pp. 543-63.Google Scholar
  19. 19.
    Altmann F, Staudacher E, Wilson IB, Marz L, Insect cells as hosts for the expression of recombinant glycoproteins, Glycoconj J 16, 109-23 (1999).PubMedCrossRefGoogle Scholar
  20. 20.
    Marchal I, Jarvis DL, Cacan R, Verbert A, Glycoproteins from insect cells: Sialylated or not? Biol Chem 382, 151-9 (2001).PubMedCrossRefGoogle Scholar
  21. 21.
    Hemmer W, Focke M, Kolarich D, Wilson IB, Altmann F, Wohrl S, Gotz M, Jarisch R, Antibody binding to venom carbohydrates is a frequent cause for double positivity to honeybee and yellow jacket venom in patients with stinging-insect allergy, J Allergy Clin Immunol 108, 1045-52 (2001).PubMedCrossRefGoogle Scholar
  22. 22.
    Wilson IB, Harthill JE, Mullin NP, Ashford DA, Altmann F, Core alpha1,3-fucose is a key part of the epitope recognized by anti-bodies reacting against plant N-linked oligosaccharides and is present in a wide variety of plant extracts, Glycobiology 8, 651-61 (1998).PubMedCrossRefGoogle Scholar
  23. 23.
    Wilson IB, Zeleny R, Kolarich D, Staudacher E, Stroop CJ, Kamerling JP, Altmann F, Analysis of Asn-linked glycans from vegetable foodstuffs: Widespread occurrence of Lewis a, core alpha1,3-linked fucose and xylose substitutions, Glycobiology 11, 261-74 (2001).PubMedCrossRefGoogle Scholar
  24. 24.
    Prenner C, Mach L, Glossl J, Marz L, The antigenicity of the carbohydrate moiety of an insect glycoprotein, honey-bee (Apis mellifera) venom phospholipase A2. The role of alpha 1,3-fucosylation of the asparagine-bound N-acetylglucosamine, Biochem J 284 (Pt2), 377-80 (1992).PubMedGoogle Scholar
  25. 25.
    Bencurova M, Hemmer W, Focke-Tejkl M, Wilson IB, Altmann F, Specificity of IgG and IgE antibodies against plant and insect glycoprotein glycans determined with artificial glycoforms of human transferrin, Glycobiology 14, 457-66 (2004).PubMedCrossRefGoogle Scholar
  26. 26.
    Tomiya N, Betenbaugh MJ, Lee YC, Humanization of lepi-dopteran insect-cell-produced glycoproteins, Acc Chem Res 36, 613-20 (2003).PubMedCrossRefGoogle Scholar
  27. 27.
    Moremen KW, Trimble RG, Herscovics A, Glycosidases of the asparagine-linked oligosaccharide processing pathway, Glycobiology 4, 113-25 (1994).PubMedGoogle Scholar
  28. 28.
    Kornfeld R, Kornfeld S, Assembly of asparagine-linked oligosac-charides, Annu Rev Biochem 54, 631-64 (1985).PubMedCrossRefGoogle Scholar
  29. 29.
    Herscovics A, Importance of glycosidases in mammalian glycoprotein biosynthesis, Biochim Biophys Acta 1473, 96-107 (1999).PubMedGoogle Scholar
  30. 30.
    Dairaku K, Spiro RG, Phylogenetic survey of endomannosidase indicates late evolutionary appearance of this N-linked oligosac-charide processing enzyme, Glycobiology 7, 579-86 (1997).PubMedGoogle Scholar
  31. 31.
    Parodi AJ, N-glycosylation in trypanosomatid protozoa, Glycobiology 3, 193-9 (1993).PubMedGoogle Scholar
  32. 32.
    Kalz-Fuller B, Bieberich E, Bause E, Cloning and expression of glucosidase I from human hippocampus, Eur J Biochem 231, 344-51 (1995).PubMedCrossRefGoogle Scholar
  33. 33.
    Spiro RG, Glucose residues as key determinants in the biosynthe-sis and quality control of glycoproteins with N-linked oligosac-charides, J Biol Chem 275, 35657-60 (2000).PubMedCrossRefGoogle Scholar
  34. 34.
    Weng S, Spiro RG, Evaluation of the early processing routes of N-linked oligosaccharides of glycoproteins through the characterization of Man8GlcNAc2 isomers: evidence that endomannosi-dase functions in vivo in the absence of a glucosidase blockade, Glycobiology 6, 861-8 (1996).PubMedGoogle Scholar
  35. 35.
    Lubas WA, Spiro RG, Evaluation of the role of rat liver Golgi endo-alpha-D-mannosidase in processing N-linked oligosaccharides, J Biol Chem 263, 3990-8 (1988).PubMedGoogle Scholar
  36. 36.
    Zuber C, Spiro MJ, Guhl B, Spiro RG, Roth J, Golgi apparatus immunolocalization of endomannosidase suggests post-endoplasmic reticulum glucose trimming: implications for quality control, Mol Biol Cell 11, 4227-40 (2000).PubMedGoogle Scholar
  37. 37.
    Tabas I, Kornfeld S, Purification and characterization of a rat liver Golgi alpha-mannosidase capable of processing asparagine-linked oligosaccharides, J Biol Chem 254, 11655-63 (1979).PubMedGoogle Scholar
  38. 38.
    Tulsiani DR, Hubbard SC, Robbins PW, Touster O, alpha-D-Mannosidases of rat liver Golgi membranes. Mannosidase II is the GlcNAcMAN5-cleaving enzyme in glycoprotein biosynthesis and mannosidases Ia and IB are the enzymes converting Man9 precursors to Man5 intermediates, J Biol Chem 257, 3660-8 (1982).PubMedGoogle Scholar
  39. 39.
    Schweden J, Legler G, Bause E, Purification and characterization of a neutral processing mannosidase from calf liver acting on(Man)9(GlcNAc)2 oligosaccharides, Eur J Biochem 157, 563-70 (1986).PubMedCrossRefGoogle Scholar
  40. 40.
    Tulsiani DR, Touster O, The purification and characterization of mannosidase IA from rat liver Golgi membranes, J Biol Chem 263, 5408-17 (1988).PubMedGoogle Scholar
  41. 41.
    Forsee WT, Palmer CF, Schutzbach JS, Purification and char-acterization of an alpha-1,2-mannosidase involved in processing asparagine-linked oligosaccharides, J Biol Chem 264, 3869-76 (1989).PubMedGoogle Scholar
  42. 42.
    Schweden J, Bause E, Characterization of trimming Man9-mannosidase from pig liver. Purification of a catalytically active fragment and evidence for the transmembrane nature of the intact 65 kDa enzyme, Biochem J 264, 347-55 (1989).PubMedGoogle Scholar
  43. 43.
    Bause E, Bieberich E, Rolfs A, Volker C, Schmidt B, Molecular cloning and primary structure of Man9-mannosidase from human kidney, Eur J Biochem 217, 535-40 (1993).PubMedCrossRefGoogle Scholar
  44. 44.
    Herscovics A, Schneikert J, Athanassiadis A, Moremen KW, Isolation of a mouse Golgi mannosidase cDNA, a member of a gene family conserved from yeast to mammals, J Biol Chem 269, 9864-71 (1994).PubMedGoogle Scholar
  45. 45.
    Lal A, Schutzbach JS, Forsee WT, Neame PJ, Moremen KW, Isolation and expression of murine and rabbit cDNAs encoding an alpha 1,2-mannosidase involved in the processing of asparagine-linked oligosaccharides, J Biol Chem 269, 9872-81 (1994).PubMedGoogle Scholar
  46. 46.
    Tremblay LO, Herscovics A, Characterization of a cDNA encoding a novel human Golgi alpha 1, 2-mannosidase (IC) involved in N-glycan biosynthesis, J Biol Chem 275, 31655-60 (2000).PubMedCrossRefGoogle Scholar
  47. 47.
    Tremblay LO, Campbell Dyke N, Herscovics A, Molecular cloning, chromosomal mapping and tissue-specific expression of a novel human alpha1,2-mannosidase gene involved in N-glycan maturation, Glycobiology 8, 585-95 (1998).PubMedCrossRefGoogle Scholar
  48. 48.
    Tremblay LO, Herscovics A, Cloning and expression of a specific human alpha 1,2-mannosidase that trims Man9GlcNAc2 to Man8GlcNAc2 isomer B during N-glycan biosynthesis, Glycobiology 9, 1073-8 (1999).PubMedCrossRefGoogle Scholar
  49. 49.
    Gonzalez DS, Karaveg K, Vandersall-Nairn AS, Lal A, Moremen KW, Identification, expression, and characterization of a cDNA encoding human endoplasmic reticulum mannosidase I, the enzyme that catalyzes the first mannose trimming step in mammalian Asn-linked oligosaccharide biosynthesis, J Biol Chem 274, 21375-86 (1999).PubMedCrossRefGoogle Scholar
  50. 50.
    Weng S, Spiro RG, Demonstration that a kifunensine-resistant alpha-mannosidase with a unique processing action on N-linked oligosaccharides occurs in rat liver endoplasmic reticulum and various cultured cells, J Biol Chem 268, 25656-63 (1993).PubMedGoogle Scholar
  51. 51.
    Weng S, Spiro RG, Endoplasmic reticulum kifunensine-resistant alpha-mannosidase is enzymatically and immunologically related to the cytosolic alpha-mannosidase, Arch Biochem Biophys 325, 113-23 (1996).PubMedCrossRefGoogle Scholar
  52. 52.
    Lal A, Pang P, Kalelkar S, Romero PA, Herscovics A, Moremen KW, Substrate specificities of recombinant murine Golgi alpha1, 2-mannosidases IA and IB and comparison with endo-plasmic reticulum and Golgi processing alpha1,2-mannosidases, Glycobiology 8, 981-95 (1998).PubMedCrossRefGoogle Scholar
  53. 53.
    Schachter H, The joys of HexNAc. The synthesis and function of N-and O-glycan branches, Glycoconj J 17, 465-83 (2000).PubMedCrossRefGoogle Scholar
  54. 54.
    Kumar R, Yang J, Larsen RD, Stanley P, Cloning and expression of N-acetylglucosaminyltransferase I, the medial Golgi transferase that initiates complex N-linked carbohydrate formation, Proc Natl Acad Sci USA 87, 9948-52 (1990).PubMedCrossRefGoogle Scholar
  55. 55.
    Kumar R, Yang J, Eddy RL, Byers MG, Shows TB, Stanley P, Cloning and expression of the murine gene and chromosomal location of the human gene encoding N-acetylglu-cosaminyltransferase I, Glycobiology 2, 383-93 (1992).PubMedGoogle Scholar
  56. 56.
    Sarkar M, Hull E, Nishikawa Y, Simpson RJ, Moritz RL, Dunn R, Schachter H, Molecular cloning and expression of cDNA encoding the enzyme that controls conversion of high-mannose to hybrid and complex N-glycans: UDP-N-acetylglucosamine: alpha-3-D-mannoside beta-1,2-N-acety-lglucosaminyltransferase I, Proc Natl Acad Sci USA 88, 234-8 (1991).PubMedCrossRefGoogle Scholar
  57. 57.
    Pownall S, Kozak CA, Schappert K, Sarkar M, Hull E, Schachter H, Marth JD, Molecular cloning and characterization of the mouse UDP-N-acetylglucosamine:alpha-3-D-mannoside beta-1,2-N-acetylglucosaminyltransferase I gene, Genomics 12, 699-704 (1992).PubMedCrossRefGoogle Scholar
  58. 58.
    Schachter H, Hull E, Sarkar M, Simpson RJ, Moritz RL, Hoppener JW, Dunn R, Molecular cloning of human and rab-bit UDP-N-acetylglucosamine: alpha-3-D-mannoside beta-1,2-N-acetylglucosaminyltransferase I, Biochem Soc Trans 19, 645-8 (1991).PubMedGoogle Scholar
  59. 59.
    Hull E, Sarkar M, Spruijt MP, Hoppener JW, Dunn R, Schachter H, Organization and localization to chromosome 5 of the human UDP-N-acetylglucosamine:alpha-3-D-mannoside beta-1,2-N-acetylglucosaminyltransferase I gene, Biochem Biophys Res Commun 176, 608-15 (1991).PubMedCrossRefGoogle Scholar
  60. 60.
    Fukada T, Iida K, Kioka N, Sakai H, Komano T, Cloning of a cDNAencoding N-acetylglucosaminyltransferase I from rat liver and analysis of its expression in rat tissues, Biosci Biotechnol Biochem 58, 200-1 (1994).PubMedCrossRefGoogle Scholar
  61. 61.
    Puthalakath H, Burke J, Gleeson PA, Glycosylation defect in Lec1 Chinese hamster ovary mutant is due to a point mutation in N-acetylglucosaminyltransferase I gene, J Biol Chem 271, 27818-22 (1996).PubMedCrossRefGoogle Scholar
  62. 62.
    Opat AS, Puthalakath H, Burke J, Gleeson PA, Genetic defect in N-acetylglucosaminyltransferase I gene of a ricin-resistant baby hamster kidney mutant, Biochem J 336 (Pt 3), 593-8 (1998).PubMedGoogle Scholar
  63. 63.
    Wilson JR, Williams D, Schachter H, The control of glycoprotein synthesis: N-acetylglucosamine linkage to a mannose residue as a signal for the attachment of L-fucose to the asparagine-linked N-acetylglucosamine residue of glycopeptide from alpha1-acid glycoprotein, Biochem Biophys Res Commun 72, 909-16 (1976).PubMedCrossRefGoogle Scholar
  64. 64.
    Longmore GD, Schachter H, Product-identification and substrate-specificity studies of the GDP-L-fucose:2-acetamido-2-deoxy-beta-D-glucoside (FUC goes to Asn-linked GlcNAc) 6-alpha-L-fucosyltransferase in a Golgi-rich fraction from porcine liver, Carbohydr Res 100, 365-92 (1982).PubMedCrossRefGoogle Scholar
  65. 65.
    Voynow JA, Kaiser RS, Scanlin TF, Glick MC, Purification and characterization of GDP-L-fucose-N-acetyl beta-D-glucosaminide alpha 1-6fucosyltransferase from cultured hu-man skin fibroblasts. Requirement of a specific biantennary oligosaccharide as substrate, J Biol Chem 266, 21572-7 (1991).PubMedGoogle Scholar
  66. 66.
    Shao MC, Sokolik CW, Wold F, Specificity studies of the GDP-[L]-fucose: 2-acetamido-2-deoxy-beta-[D]-glucoside (Fuc→Asn-linked GlcNAc) 6-alpha-[L]-fucosyltransferase from rat-liver Golgi membranes, Carbohydr Res 251, 163-73 (1994).PubMedCrossRefGoogle Scholar
  67. 67.
    Moremen KW, Golgi alpha-mannosidase II deficiency in vertebrate systems: Implications for asparagine-linked oligosaccha-ride processing in mammals, Biochim Biophys Acta 1573, 225-35 (2002).PubMedGoogle Scholar
  68. 68.
    Harpaz N, Schachter H, Control of glycoprotein synthesis. Pro-cessing of asparagine-linked oligosaccharides by one or more rat liver Golgi alpha-D-mannosidases dependent on the prior action of UDP-N-acetylglucosamine: Alpha-D-mannoside beta 2-N-acetylglucosaminyltransferase I, J Biol Chem 255, 4894-902 (1980).PubMedGoogle Scholar
  69. 69.
    Velasco A, Hendricks L, Moremen KW, Tulsiani DR, Touster O, Farquhar MG, Cell type-dependent variations in the subcellular distribution of alpha-mannosidase I and II, J Cell Biol 122, 39-51 (1993).PubMedCrossRefGoogle Scholar
  70. 70.
    Moremen KW, Touster O, Robbins PW, Novel purification of the catalytic domain of Golgi alpha-mannosidase II. Characterization and comparison with the intact enzyme, J Biol Chem 266, 16876-85 (1991).PubMedGoogle Scholar
  71. 71.
    Tulsiani DR, Opheim DJ, Touster O, Purification and characteri-zation of alpha-D-mannosidase from rat liver golgi membranes, J Biol Chem 252, 3227-33 (1977).PubMedGoogle Scholar
  72. 72.
    Kaushal GP, Szumilo T, Pastuszak I, Elbein AD, Purification to homogeneity and properties of mannosidase II from mung bean seedlings, Biochemistry 29, 2168-76 (1990).PubMedCrossRefGoogle Scholar
  73. 73.
    Misago M, Liao YF, Kudo S, Eto S, Mattei MG, Moremen KW, Fukuda MN, Molecular cloning and expression of cDNAs encoding human alpha-mannosidase II and a previously unrecognized alpha-mannosidase IIx isozyme, Proc Natl Acad Sci USA 92, 11766-70 (1995).PubMedCrossRefGoogle Scholar
  74. 74.
    Moremen KW, Isolation of a rat liver Golgi mannosidase II clone by mixed oligonucleotide-primed amplification of cDNA, Proc Natl Acad Sci USA 86, 5276-80 (1989).PubMedCrossRefGoogle Scholar
  75. 75.
    Moremen KW, Robbins PW, Isolation, characterization, and expression of cDNAs encoding murine alpha-mannosidase II, a Golgi enzyme that controls conversion of high mannose to complex N-glycans, J Cell Biol 115, 1521-34 (1991).PubMedCrossRefGoogle Scholar
  76. 76.
    Rabouille C, Kuntz DA, Lockyer A, Watson R, Signorelli T, Rose DR, van den Heuvel M, Roberts DB, The Drosophila GMII gene encodes a Golgi alpha-mannosidase II, J Cell Sci 112 (Pt 19), 3319-30 (1999).PubMedGoogle Scholar
  77. 77.
    Foster JM, Yudkin B, Lockyer AE, Roberts DB, Cloning and sequence analysis of GmII, a Drosophila melanogaster homologue of the cDNA encoding murine Golgi alpha-mannosidase II, Gene 154, 183-6 (1995).PubMedCrossRefGoogle Scholar
  78. 78.
    Bonay P, Hughes RC, Purification and characterization of a novel broad-specificity (alpha 1-2, alpha 1-3 and alpha 1-6) man-nosidase from rat liver, Eur J Biochem 197, 229-38 (1991).PubMedCrossRefGoogle Scholar
  79. 79.
    Bonay P, Roth J, Hughes RC, Subcellular distribution in rat liver of a novel broad-specificity (alpha 1-2, alpha 1-3 and alpha 1-6) mannosidase active on oligomannose glycans, Eur J Biochem 205, 399-407 (1992).PubMedCrossRefGoogle Scholar
  80. 80.
    Chui D, Oh-Eda M, Liao YF, Panneerselvam K, Lal A, Marek KW, Freeze HH, Moremen KW, Fukuda MN, Marth JD, Alpha-mannosidase-II deficiency results in dyserythropoiesis and un-veils an alternate pathway in oligosaccharide biosynthesis, Cell 90, 157-67 (1997).PubMedCrossRefGoogle Scholar
  81. 81.
    Oh-Eda M, Nakagawa H, Akama TO, Lowitz K, Misago M, Moremen KW, Fukuda MN, Overexpression of the Golgi-localized enzyme alpha-mannosidase IIx in Chinese hamster ovary cells results in the conversion of hexamannosyl-N-acetylchitobiose to tetramannosyl-N-acetylchitobiose in the N-glycan-processing pathway, Eur J Biochem 268, 1280-8 (2001).PubMedCrossRefGoogle Scholar
  82. 82.
    Schachter H, Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides, Biochem Cell Biol 64, 163-81 (1986).PubMedCrossRefGoogle Scholar
  83. 83.
    Schachter H, The 'yellow brick road' to branched complex N-glycans, Glycobiology 1, 453-61 (1991).PubMedGoogle Scholar
  84. 84.
    Tulsiani DR, Touster O, Characterization of a novel alpha-D-mannosidase from rat brain microsomes, J Biol Chem 260, 13081-7 (1985).PubMedGoogle Scholar
  85. 85.
    Tan J, D'Agostaro AF, Bendiak B, Reck F, Sarkar M, Squire JA, Leong P, Schachter H, The human UDP-N-acetylglucosamine: Alpha-6-D-mannoside-beta-1,2-N-acetyl-glucosaminyltransferase II gene (MGAT2). Cloning of genomic DNA, localization to chromosome 14q21, expression in insect cells and purification of the recombinant protein, Eur J Biochem 231, 317-28 (1995).PubMedCrossRefGoogle Scholar
  86. 86.
    D'Agostaro GA, Zingoni A, Moritz RL, Simpson RJ, Schachter H, Bendiak B, Molecular cloning and expression of cDNA encoding the rat UDP-N-acetylglucosamine:alpha-6-D-mannoside beta-1,2-N-acetylglucosaminyltransferase II, J Biol Chem 270, 15211-21 (1995).PubMedCrossRefGoogle Scholar
  87. 87.
    Furukawa K, Sato T, Beta-1,4-galactosylation of N-glycans is a complex process, Biochim Biophys Acta 1473, 54-66 (1999).PubMedGoogle Scholar
  88. 88.
    Hennet T, The galactosyltransferase family, Cell Mol Life Sci 59, 1081-95 (2002).PubMedCrossRefGoogle Scholar
  89. 89.
    Guo S, Sato T, Shirane K, Furukawa K, Galactosylation of N-linked oligosaccharides by human beta-1,4-galactosyltransferases I, II, III, IV, V, and VI expressed in Sf-9 cells, Glycobiology 11, 813-20 (2001).PubMedCrossRefGoogle Scholar
  90. 90.
    Harduin-Lepers A, Vallejo-Ruiz V, Krzewinski-Recchi MA, Samyn-Petit B, Julien S, Delannoy P, The human sialyltrans-ferase family, Biochimie 83, 727-37 (2001).PubMedCrossRefGoogle Scholar
  91. 91.
    Tsuji S, Datta AK, Paulson JC, Systematic nomenclature for sialyltransferases, Glycobiology 6, v-vii (1996).PubMedGoogle Scholar
  92. 92.
    Grundmann U, Nerlich C, Rein T, Zettlmeissl G, Complete cDNA sequence encoding human beta-galactoside alpha-2,6-sialyltransferase, Nucleic Acids Res 18, 667 (1990).PubMedGoogle Scholar
  93. 93.
    Takashima S, Tsuji S, Tsujimoto M, Characterization of the sec-ond type of human beta-galactoside alpha 2,6-sialyltransferase (ST6Gal II), which sialylates Galbeta 1,4GlcNAc structures on oligosaccharides preferentially. Genomic analysis of human sialyltransferase genes, J Biol Chem 277, 45719-28 (2002).PubMedCrossRefGoogle Scholar
  94. 94.
    Krzewinski-Recchi MA, Julien S, Juliant S, Teintenier-Lelievre M, Samyn-Petit B, Montiel MD, Mir AM, Cerutti M, Harduin-Lepers A, Delannoy P, Identification and functional expression of a second human beta-galactoside alpha2,6-sialyltransferase, ST6Gal II, Eur J Biochem 270, 950-61 (2003).PubMedCrossRefGoogle Scholar
  95. 95.
    Ailor E, Takahashi N, Tsukamoto Y, Masuda K, Rahman BA, Jarvis DL, Lee YC, Betenbaugh MJ, N-glycan patterns of human transferrin produced in Trichoplusia ni insect cells: Effects of mammalian galactosyltransferase, Glycobiology 10, 837-47 (2000).PubMedCrossRefGoogle Scholar
  96. 96.
    Davis TR, Schuler ML, Granados RR, Wood HA, Comparison of oligosaccharide processing among various insect cell lines expressing a secreted glycoprotein, In Vitro Cellular & Developmental Biology Animal 29A, 842-6 (1993).Google Scholar
  97. 97.
    Ren J, Bretthauer RK, Castellino FJ, Purification and properties of a Golgi-derived (alpha 1,2)-mannosidase-I from baculovirus-infected lepidopteran insect cells (IPLB-SF21AE) with preferential activity toward mannose6-N-acetylglucosamine2, Biochemistry 34, 2489-95 (1995).PubMedCrossRefGoogle Scholar
  98. 98.
    Kawar Z, Herscovics A, Jarvis DL, Isolation and characterization of an alpha 1,2-mannosidase cDNA from the lepidopteran insect cell line Sf9, Glycobiology 7, 433-43 (1997).PubMedGoogle Scholar
  99. 99.
    Kawar Z, Romero PA, Herscovics A, Jarvis DL, N-Glycan processing by a lepidopteran insect alpha1,2-mannosidase, Glycobiology 10, 347-55 (2000).PubMedCrossRefGoogle Scholar
  100. 100.
    Kawar Z, Jarvis DL, Biosynthesis and subcellular localization of a lepidopteran insect alpha 1,2-mannosidase, Insect Biochem Mol Biol 31, 289-97 (2001).PubMedCrossRefGoogle Scholar
  101. 101.
    Altmann F, Kornfeld G, Dalik T, Staudacher E, Glossl J, Processing of asparagine-linked oligosaccharides in in-sect cells. N-acetylglucosaminyltransferase I and II activities in cultured lepidopteran cells, Glycobiology 3, 619-25 (1993).PubMedGoogle Scholar
  102. 102.
    Velardo MA, Bretthauer RK, Boutaud A, Reinhold B, Reinhold VN, Castellino FJ, The presence of UDP-N-acetylglucosamine: alpha-3-D-mannoside beta 1,2-N-acetylglucosaminyltransferase I activity in Spodoptera frugiperda cells (IPLB-SF-21AE) and its enhancement as a result of baculovirus infection, J Biol Chem 268, 17902-7 (1993).PubMedGoogle Scholar
  103. 103.
    Sarkar M, Schachter H, Cloning and expression of Drosophila melanogaster UDP-GlcNAc: alpha-3-D-mannoside beta1,2-N-acetylglucosaminyltransferase I, Biol Chem 382, 209-17 (2001).PubMedCrossRefGoogle Scholar
  104. 104.
    Altmann F, Marz L, Processing of asparagine-linked oligosaccharides in insect cells: Evidence for á-mannosidase II, Glycoconj J 12, 150-5 (1995).PubMedCrossRefGoogle Scholar
  105. 105.
    Ren J, Castellino FJ, Bretthauer RK, Purification and prop-erties of alpha-mannosidase II from Golgi-like membranes of baculovirus-infected Spodoptera frugiperda (IPLB-SF-21 AE) cells., Biochem J 15, 951-6 (1997).Google Scholar
  106. 106.
    Kawar Z, Karaveg K, Moremen KW, Jarvis DL, Insect cells encode a class II alpha-mannosidase with unique properties, Journal of Biological Chemistry 276, 16335-40 (2001).PubMedCrossRefGoogle Scholar
  107. 107.
    Jarvis DL, Bohlmeyer DA, Liao YF, Lomax KK, Merkle RK, Weinkauf C, Moremen KW, Isolation and characterization of a class II alpha-mannosidase cDNA from lepidopteran insect cells, Glycobiology 7, 113-27 (1997).PubMedGoogle Scholar
  108. 108.
    Tsitilou SG, Grammenoudi S, Evidence for alternative splicing and developmental regulation of the Drosophila melanogaster Mgat2 (N-acetylglucosaminyltransferase II) gene, Biochem Biophys Res Commun 312, 1372-6 (2003).PubMedCrossRefGoogle Scholar
  109. 109.
    Schachter H, N-Acetylglucosaminyltransferase-II. In Handbook of GLycosyltransferases and Related Genes,Vol., edited by Taniguchi K, Honke K, Fukuda M (Springer-Verlag, Tokyo, Japan, 2002), pp. 70-9.Google Scholar
  110. 110.
    Hollister JR, Shaper JH, Jarvis DL, Stable expression of mammalian beta 1, 4-galactosyltransferase extends the N-glycosylation pathway in insect cells, Glycobiology 8, 473-80 (1998).PubMedCrossRefGoogle Scholar
  111. 111.
    van Die I, van Tetering A, Bakker H, van den Eijnden DH, Joziasse DH, Glycosylation in lepidopteran insect cells: Identification of a beta 1→4-N-acetylgalactosaminyltransferase involved in the synthesis of complex-type oligosaccharide chains, Glycobiology 6, 157-64 (1996).PubMedGoogle Scholar
  112. 112.
    Hollister JR, Jarvis DL, Engineering lepidopteran insect cells for sialoglycoprotein production by genetic transformation with mammalian beta 1,4-galactosyltransferase and alpha 2,6-sialyltransferase genes, Glycobiology 11, 1-9 (2001).PubMedCrossRefGoogle Scholar
  113. 113.
    Abdul-Rahman B, Ailor E, Jarvis D, Betenbaugh M, Lee YC, Beta-(1→4)-galactosyltransferase activity in native and engineered insect cells measured with time-resolved europium fluorescence, Carbohydr Res 337, 2181-6 (2002).PubMedCrossRefGoogle Scholar
  114. 114.
    Vadaie N, Jarvis DL, Molecular cloning and functional characterization of a lepidopteran insect beta 4-N-acetyl-galactosaminyltransferase with broad substrate specificity, a functional role in N-glycoprotein biosynthesis, and a potential functional role in glycolipid biosynthesis, J Biol Chem (2004).Google Scholar
  115. 115.
    Lopez M, Tetaert D, Juliant S, Gazon M, Cerutti M, Verbert A, Delannoy P, O-glycosylation potential of lepidopteran insect cell lines, Biochim Biophys Acta 1427, 49-61 (1999).PubMedGoogle Scholar
  116. 116.
    Hooker AD, Green NH, Baines AJ, Bull AT, Jenkins N, Strange PG, James DC, Constraints on the transport and glycosylation of recombinant IFN-gamma in Chinese hamster ovary and insect cells, Biotechnol Bioeng 63, 559-72 (1999).PubMedCrossRefGoogle Scholar
  117. 117.
    Roth J, Kempf A, Reuter G, Schauer R, Gehring WJ, Occurrence of sialic acids in Drosophila melanogaster, Science 256, 673-5 (1992).PubMedGoogle Scholar
  118. 118.
    Malykh YN, Krisch B, Gerardy-Schahn R, Lapina EB, Shaw L, Schauer R, The presence of N-acetylneuraminic acid in Malpighian tubules of larvae of the cicada Philaenus spumarius, Glycoconj J 16, 731-9 (1999).PubMedCrossRefGoogle Scholar
  119. 119.
    Koles K, Irvine KD, Panin VM, Functional characterization of Drosophila sialyltransferase, J Biol Chem 279, 4346-57 (2004).PubMedCrossRefGoogle Scholar
  120. 120.
    Davidson DJ, Castellino FJ, Asparagine-linked oligosaccharide processing in lepidopteran insect cells. Temporal dependence of the nature of the oligosaccharides assembled on asparagine-289 of recombinant human plasminogen produced in baculovirus vector infected Spodoptera frugiperda (IPLB-SF-21AE) cells, Bio-chemistry 30, 6165-74 (1991).Google Scholar
  121. 121.
    Davidson DJ, Castellino FJ, Structures of the asparagine-289-linked oligosaccharides assembled on recombinant human plas-minogen expressed in a Mamestra brassicae cell line (IZD-MBO503), Biochemistry 30, 6689-96 (1991).PubMedCrossRefGoogle Scholar
  122. 122.
    Palomares LA, Joosten CE, Hughes PR, Granados RR, Shuler ML, Novel insect cell line capable of complex N-glycosylation and sialylation of recombinant proteins, Biotechnol Prog 19, 185-92 (2003).PubMedCrossRefGoogle Scholar
  123. 123.
    Altmann F, Schwihla H, Staudacher E, Glossl J, Marz L, Insect cells contain an unusual, membrane-bound beta-N-acetylglucosaminidase probably involved in the processing of protein N-glycans, J Biol Chem 270, 17344-9 (1995).PubMedCrossRefGoogle Scholar
  124. 124.
    Licari PJ, Jarvis DL, Bailey JE, Insect cell hosts for baculovirus expression vectors contain endogenous exoglycosidase activity, Biotechnol Prog 9, 146-52 (1993).PubMedCrossRefGoogle Scholar
  125. 125.
    Bendiak B, Schachter H, Control of glycoprotein synthesis. Kinetic mechanism, substrate specificity, and inhibition characteristics of UDP-N-acetylglucosamine:alpha-D-mannoside beta 1-2 N-acetylglucosaminyltransferase II from rat liver, J Biol Chem 262, 5784-90 (1987).PubMedGoogle Scholar
  126. 126.
    Staudacher E, Marz L, Strict order of (Fuc to Asn-linked Glc-NAc) fucosyltransferases forming core-difucosylated structures, Glycoconj J 15, 355-60 (1998).PubMedCrossRefGoogle Scholar
  127. 127.
    Takahashi N, Tsukamoto Y, Shiosaka S, Kishi T, Hakoshima T, Arata Y, Yamaguchi Y, Kato K, Shimada I, N-glycan structures of murine hippocampus serine protease, neuropsin, produced in Trichoplusia ni cells, Glycoconj J 16, 405-14 (1999).PubMedCrossRefGoogle Scholar
  128. 128.
    Rudd PM, Downing AK, Cadene M, Harvey DJ, Wormald MR, Weir I, Dwek RA, Rifkin DB, Gleizes PE, Hybrid and complex glycans are linked to the conserved N-glycosylation site of the third eight-cysteine domain of LTBP-1 in insect cells, Biochemistry 39, 1596-603 (2000).PubMedCrossRefGoogle Scholar
  129. 129.
    Staudacher E, Kubelka V, Marz L, Distinct N-glycan fucosylation potentials of three lepidopteran cell lines, Eur J Biochem 207, 987-93 (1992).PubMedCrossRefGoogle Scholar
  130. 130.
    Fabini G, Freilinger A, Altmann F, Wilson IB, Identification of core alpha 1,3-fucosylated glycans and cloning of the requisite fucosyltransferase cDNA from Drosophila melanogaster. Potential basis of the neural anti-horseradish peroxidase epitope, J Biol Chem 276, 28058-67 (2001).PubMedCrossRefGoogle Scholar
  131. 131.
    Tomiya N, Ailor E, Lawrence SM, Betenbaugh MJ, Lee YC, 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, 129-37 (2001).PubMedCrossRefGoogle Scholar
  132. 132.
    Hinderlich S, Stasche R, Zeitler R, Reutter W, A bifunctional enzyme catalyzes the first two steps in N-acetylneuraminic acid biosynthesis of rat liver. Purification and characterization of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase, J Biol Chem 272, 24313-8 (1997).PubMedCrossRefGoogle Scholar
  133. 133.
    Effertz K, Hinderlich S, Reutter W, 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, 28771-8 (1999).PubMedCrossRefGoogle Scholar
  134. 134.
    Lawrence SM, Huddleston KA, Tomiya N, Nguyen N, Lee YC, Vann WF, Coleman TA, Betenbaugh MJ, Cloning and expression of human sialic acid pathway genes to generate CMP-sialic acids in insect cells, Glycoconj J 18, 205-13 (2001).PubMedCrossRefGoogle Scholar
  135. 135.
    Lawrence SM, Huddleston KA, Pitts LR, Nguyen N, Lee YC, Vann WF, Coleman TA, Betenbaugh MJ, Cloning and expression of the human N-acetylneuraminic acid phosphate synthase gene with 2-keto-3-deoxy-D-glycero-D-galactonononic acid biosynthetic ability, J Biol Chem 275, 17869-77 (2000).PubMedCrossRefGoogle Scholar
  136. 136.
    Joshi L, Davis TR, Mattu TS, Rudd PM, Dwek RA, Shuler ML, Wood HA, Influence of baculovirus-host cell interactions on complex N-linked glycosylation of a recombinant human protein, Biotechnol Prog 16, 650-6 (2000).PubMedCrossRefGoogle Scholar
  137. 137.
    Ogonah OW, Freedman RB, Jenkins N, Rooney BC, Analysis of human interferon-gamma glycoforms produced in baculovirus infected insect cells by matrix assisted laser desorption spectrometry, Biochem Soc Trans 23, 100S (1995).Google Scholar
  138. 138.
    Wathen MW, Aeed PA, Elhammer AP, Characterization of oligosaccharide structures on a chimeric respiratory syncytial virus protein expressed in insect cell line Sf9, Biochemistry 30, 2863-8 (1991).PubMedCrossRefGoogle Scholar
  139. 139.
    Wagner R, Geyer H, Geyer R, Klenk H-D, N-acetyl-.beta.-glucosaminidase accounts for differences in glycosylation of influenza virus hemagglutinin expressed in insect cells from a baculovirus vector, Journal of Virology 70, 4103-9 (1996).PubMedGoogle Scholar
  140. 140.
    Watanabe S, Kokuho T, Takahashi H, Takahashi M, Kubota T, Inumaru S, Sialylation of N-glycans on the recombinant proteins expressed by a baculovirus-insect cell system under beta-N-acetylglucosaminidase inhibition, J Biol Chem 277, 5090-3 (2002).PubMedCrossRefGoogle Scholar
  141. 141.
    Jarvis DL, Finn EE, Modifying the insect cell N-glycosylation pathway with immediate early baculovirus expression vectors, Nat Biotechnol 14, 1288-92 (1996).PubMedCrossRefGoogle Scholar
  142. 142.
    Wolff MW, Murhammer DW, Jarvis DL, Linhardt RJ, Electrophoretic analysis of glycoprotein glycans produced by lepidopteran insect cells infected with an immediate early recombinant baculovirus encoding mam-malian beta1,4-galactosyltransferase, Glycoconj J 16, 753-6 (1999).CrossRefGoogle Scholar
  143. 143.
    Breitbach K, Jarvis DL, Improved glycosylation of a foreign pro-tein by Tn-5B1-4 cells engineered to express mammalian glyco-syltransferases, Biotechnol Bioeng 74, 230-9 (2001).PubMedCrossRefGoogle Scholar
  144. 144.
    Hollister J, Grabenhorst E, Nimtz M, Conradt H, Jarvis DL, Engineering the protein N-glycosylation pathway in insect cells for production of biantennary, complex N-glycans, Biochemistry 41, 15093-104 (2002).PubMedCrossRefGoogle Scholar
  145. 145.
    Tomiya N, Howe D, Aumiller JJ, Pathak M, Park J, Palter K, Jarvis DL, Betenbaugh MJ, Lee YC, Complex-type biantennary N-glycans of recombinant human transferrin from Trichoplusia ni insect cells expressing mammalian â-1,4-galactosyltransferase and â-1,2-N-acetylglucosaminyltransferase II, Glycobiology 13, 23-34 (2003).PubMedCrossRefGoogle Scholar
  146. 146.
    Tomiya N, Suzuki T, Awaya J, Mizuno K, Matsubara A, Nakano K, Kurono M, Determination of monosaccharides and sugar alcohols in tissues from diabetic rats by high-performance liquid chromatography with pulsed amperometric detection, Anal Biochem 206, 98-104 (1992).PubMedCrossRefGoogle Scholar
  147. 147.
    Annunziato PW, Wright LF, Vann WF, Silver RP, Nucleotide sequence and genetic analysis of the neuD and neuB genes in region 2 of the polysialic acid gene cluster of Escherichia coli K1, J Bacteriol 177, 312-9 (1995).PubMedGoogle Scholar
  148. 148.
    Zapata G, Crowley JM, Vann WF, Sequence and expression of the Escherichia coli K1 neuC gene product, J Bacteriol 174, 315-9 (1992).PubMedGoogle Scholar
  149. 149.
    Viswanathan K, Lawrence S, Hinderlich S, Yarema KJ, Lee YC, Betenbaugh MJ, Engineering sialic acid synthetic ability into insect cells: Identifying metabolic bottlenecks and devis-ing strategies to overcome them, Biochemistry 42, 15215-25 (2003).PubMedCrossRefGoogle Scholar
  150. 150.
    Jarvis DL, Howe D, Aumiller JJ, Novel baculovirus expression vectors that provide sialylation of recombinant glycoproteins in lepidopteran insect cells, J Virol 75, 6223-7 (2001).PubMedCrossRefGoogle Scholar
  151. 151.
    Seo N-S, Hollister JR, Jarvis DL, Mammalian glycosyl-transferase expression allows sialoglycoprotein production by baculovirus-infected insect cells, Protein Expression and Purification 22, 234-41 (2001).PubMedCrossRefGoogle Scholar
  152. 152.
    Hollister J, Conradt H, Jarvis DL, Evidence for a Sialic Acid Salvaging Pathway in Lepidopteran Insect Cells, Glycobiology 13, 487-95 (2003).PubMedCrossRefGoogle Scholar
  153. 153.
    Chang GD, Chen CJ, Lin CY, Chen HC, Chen H, Improvement of glycosylation in insect cells with mammalian glycosyltrans-ferases, J Biotechnol 102, 61-71 (2003).CrossRefGoogle Scholar
  154. 154.
    Jarvis DL, Hollister J, Aumiller JJ, Development of Novel Transgenic Insect Cell Lines that support humanized glycoprotein production by baculovirus expression vectors, Bioprocessing Journal 30-4 (2003).Google Scholar
  155. 155.
    Aumiller JJ, Hollister JR, Jarvis DL, A Transgenic Insect Cell Line Engineered to Produce CMP-Sialic Acid and Sialylated Glycoproteins, Glycobiology 13, 497-507 (2003).PubMedCrossRefGoogle Scholar
  156. 156.
    Joshi L, Shuler ML, Wood HA, Production of a sialylated N-linked glycoprotein in insect cells, Biotechnol Prog 17, 822-7 (2001).PubMedCrossRefGoogle Scholar
  157. 157.
    Joosten CE, Shuler ML, Effect of culture conditions on the degree of sialylation of a recombinant glycoprotein expressed in insect cells, Biotechnol Prog 19, 739-49 (2003).PubMedCrossRefGoogle Scholar
  158. 158.
    Joosten CE, Park TH, Shuler ML, Effect of silkworm hemolymph on N-linked glycosylation in two Trichoplusia ni insect cell lines, Biotechnol Bioeng 83, 695-705 (2003).PubMedCrossRefGoogle Scholar
  159. 159.
    Angata T, Varki A, 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, 22127-35 (2000).PubMedCrossRefGoogle Scholar
  160. 160.
    Kim K, Lawrence SM, Park J, Pitts L, Vann WF, Betenbaugh MJ, Palter KB, 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 (2002).PubMedCrossRefGoogle Scholar
  161. 161.
    Staudacher E, Altmann F, Wilson IB, Marz L, Fucose in N-glycans: from plant to man, Biochim Biophys Acta 1473, 216-36 (1999).PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Noboru Tomiya
    • 1
  • Someet Narang
    • 2
  • Yuan C. Lee
    • 1
  • Michael J. Betenbaugh
    • 2
  1. 1.Department of BiologyJohns Hopkins UniversityBaltimoreUSA
  2. 2.Department of Chemical and Biomolecular EngineeringJohns Hopkins UniversityBaltimoreUSA

Personalised recommendations