A novel baculovirus vector for the production of nonfucosylated recombinant glycoproteins in insect cells

Glycobiology

Volumn 24, Issue 3, 2014, Pages 325-340

  Mabashi Asazuma, Hideaki ^a   Kuo, Chu Wei ^b   Khoo, Kay Hooi ^b   Jarvis, Donald L ^a  

^a UNIVERSITY OF WYOMING   (United States)

^b INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

Author keywords

baculovirus; fucosylation; glycoengineering; glycoprotein production; insect cells

Indexed keywords

BACULOVIRUS; FUCOSYLATION; GLYCOENGINEERING; GLYCOPROTEIN PRODUCTION; INSECT CELLS;

ANIMALS; BACTERIAL PROTEINS; BACULOVIRIDAE; BIOTECHNOLOGY; FUCOSE; GENETIC VECTORS; GLYCOPROTEINS; KETONE OXIDOREDUCTASES; PSEUDOMONAS AERUGINOSA; RECOMBINANT PROTEINS; SF9 CELLS; SPODOPTERA;

EID: 84894282237     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt161     Document Type: Article

References (92)

1. Ailor E, Takahashi N, Tsukamoto Y, Masuda K, Rahman BA, Jarvis DL, Lee YC, Betenbaugh MJ. 2000. N-glycan patterns of human transferrin produced in Trichoplusia ni insect cells: Effects of mammalian galactosyltransferase. Glycobiology. 10:837-847.
2. Altmann F. 2007. The role of protein glycosylation in allergy. Int Arch Allergy Immunol. 142:99-115.
3. Aumiller JJ, Hollister JR, Jarvis DL. 2003. A transgenic insect cell line engineered to produce CMP-sialic acid and sialylated glycoproteins. Glycobiology. 13:497-507.
4. Aumiller JJ, Mabashi-Asazuma H, Hillar A, Shi X, Jarvis DL. 2012. A new glycoengineered insect cell line with an inducibly mammalianized protein N-glycosylation pathway. Glycobiology. 22:417-428.
5. Bao S, Cagan R. 2006. Fast cloning inverted repeats for RNA interference. RNA. 12:2020-2024.
6. Blake MS, Johnston KH, Russell-Jones GJ, Gotschlich EC. 1984. A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody onWestern blots. Analyt Biochem. 136:175-179.
7. Blank S, Michel Y, Seismann H, Plum M, Greunke K, Grunwald T, Bredehorst R, Ollert M, Braren I, Spillner E. 2011. Evaluation of different glycoforms of honeybee venom major allergen phospholipase A2 (Api m 1) produced in insect cells. Prot Pept Lett. 18:415-422.
8. Bongiovanni A, Romancino DP, Campos Y, Paterniti G, Qiu X, Moshiach S, Di FV, Vergani N, Ustek D, d'Azzo A. 2012. Alix protein is substrate of Ozz-E3 ligase and modulates actin remodeling in skeletal muscle. J Biol Chem. 287:12159-12171.
9. Bourhis E, Tam C, Franke Y, Bazan JF, Ernst J, Hwang J, Costa M, Cochran AG, Hannoush RN. 2010. Reconstitution of a frizzled8·Wnt3a·LRP6 signaling complex reveals multiple Wnt and Dkk1 binding sites on LRP6. J Biol Chem. 285:9172-9179.
10. Bozon V, Remy JJ, Pajot-Augy E, Couture L, Biache G, Severini M, Salesse R. 1995. Influence of promoter and signal peptide on the expression and secretion of recombinant porcine LH extracellular domain in baculovirus/ lepidopteran cells or the caterpillar system. J Mol Endocrinol. 14:277-284.
11. Breitbach K, Jarvis DL. 2001. Improved glycosylation of a foreign protein by Tn-5B1-4 cells engineered to express mammalian glycosyltransferases. Biotechnol Bioeng. 74:230-239.
12. Cérutti M, Golay J. 2012. Lepidopteran cells, an alternative for the production of recombinant antibodies? MAbs. 4:294-309.
13. Chang GD, Chen CJ, Lin CY, Chen HC, Chen H. 2003. Improvement of glycosylation in insect cells with mammalian glycosyltransferases. J Biotechnol. 102:61-71.
14. Davis TR, Trotter KM, Granados RR, Wood HA. 1992. Baculovirus expression of alkaline phosphatase as a reporter gene for evaluation of production, glycosylation and secretion. Nat Biotechnol. 10:1148-1150.
15. Dee KU, Shuler ML, Wood HA. 1997. Inducing single-cell suspension of BTI-TN5B1-4 insect cells: I. The use of sulfated polyanions to prevent cell aggregation and enhance recombinant protein production. Biotechnol Bioeng. 54:191-205.
16. Dell A, Reason AJ, Khoo KH, Panico M, McDowell RA, Morris HR. 1994. Mass spectrometry of carbohydrate-containing biopolymers. Meth Enzymol. 230:108-132.
17. Elvin JG, Couston RG, van CF. 2013. Therapeutic antibodies: Market considerations, disease targets and bioprocessing. Int J Pharm. 440:83-98.
18. Fabini G, Freilinger A, Altmann F, Wilson IB. 2001. Identification of core a1,3-fucosylated glycans and cloning of the requisite fucosyltransferase cDNA from Drosophila melanogaster. Potential basis of the neural antihorseadish peroxidase epitope. J Biol Chem. 276:28058-28067.
19. Ferrara C, Brunker P, Suter T, Moser S, Puntener U, Umana P. 2006. Modulation of therapeutic antibody effector functions by glycosylation engineering: Influence of Golgi enzyme localization domain and co-expression of heterologous ß1,4-N-acetylglucosaminyltransferase III and Golgi alphamannosidase II. Biotechnol Bioeng. 93:851-861.
20. Fötisch K, Viehs S. 2001. N-and O-linked oligosaccharides of allergenic glycoproteins. Glycoconj J. 18:373-390.
21. Geisler C, Aumiller JJ, Jarvis DL. 2008. A fused lobes gene encodes the processing ß-N-acetylglucosaminidase in Sf9 cells. J Biol Chem. 283:11330-11339.
22. Geisler C, Jarvis DL. 2012. Innovative use of a bacterial enzyme involved in sialic acid degradation to initiate sialic acid biosynthesis in glycoengineered insect cells. Metab Eng. 14:642-652.
23. Guarino LA, Summers MD. 1986. Functional mapping of a trans-activating gene required for expression of a baculovirus delayed-early gene. J Virol. 57:563-571.
24. Hancock K, Narang S, Pattabhi S, Yushak ML, Khan A, Lin SC, Plemons R, Betenbaugh MJ, Tsang VC. 2008. False positive reactivity of recombinant, diagnostic, glycoproteins produced in High Five insect cells: Effect of glycosylation. J Immunol Meth. 330:130-136.
25. Harrison RL, Jarvis DL. 2007. Transforming lepidopteran insect cells for continuous recombinant protein expression. Meth Mol Biol. 388:299-316.
26. Hawtin RE, Zarkowska T, Arnold K, Thomas CJ, Gooday GW, King LA, Kuzio JA, Possee RD. 1997. Liquefaction of Autographa californica nucleopolyhedrovirusinfected insects is dependent on the integrity of virus-encoded chitinase and cathepsin genes. Virology. 238:243-253.
27. He CH, Lee CG, Dela CCS, Lee CM, Zhou Y, Ahangari F, Ma B, Herzog EL, Rosenberg SA, Li Y, et al. 2013. Chitinase 3-like 1 regulates cellular and tissue responses via IL-13 receptor a2. Cell Rep. 4:830-841.
28. Hill DR, Aumiller JJ, Shi X, Jarvis DL. 2006. Isolation and analysis of a baculovirus vector that supports recombinant glycoprotein sialylation by SfSWT-1 cells cultured in serum-free medium. Biotechnol Bioeng. 95:37-47.
29. Hillar A, Jarvis DL. 2010. Re-visiting the endogenous capacity for recombinant glycoprotein sialylation by baculovirus-infected Tn-4 h and DpN1 cells. Glycobiology. 20:1323-1330.
30. Hitchman RB, Possee RD, Siaterli E, Richards KS, Clayton AJ, Bird LE, Owens RJ, Carpentier DC, King FL, Danquah JO, et al. 2010. Improved expression of secreted and membrane-targeted proteins in insect cells. Biotechnol Appl Biochem. 56:85-93.
31. Hollister JR, Grabenhorst E, Nimtz M, Conradt H, Jarvis DL. 2002. Engineering the protein N-glycosylation pathway in insect cells for production of biantennary, complex N-glycans. Biochemistry. 41:15093-15104.
32. Hollister JR, Jarvis DL. 2001. Engineering lepidopteran insect cells for sialoglycoprotein production by genetic transformation with mammalian ß1,4-galactosyltransferase and a2,6-sialyltransferase genes. Glycobiology. 11:1-9.
33. Hollister JR, Shaper JH, Jarvis DL. 1998. Stable expression of mammalian ß1,4-galactosyltransferase extends the N-glycosylation pathway in insect cells. Glycobiology. 8:473-480.
34. Imai-Nishiya H, Mori K, Inoue M, Wakitani M, Iida S, Shitara K, Satoh M. 2007. Double knockdown of a1,6-fucosyltransferase (FUT8) and GDP-mannose 4,6-dehydratase (GMD) in antibody-producing cells: A new strategy for generating fully non-fucosylated therapeutic antibodies with enhanced ADCC. BMC Biotechnol. 7:84.
35. Jarvis DL. 2009. Baculovirus-insect cell expression systems. Meth Enzymol. 463:191-222.
36. Jarvis DL, Finn EE. 1996. Modifying the insect cell N-glycosylation pathway with immediate early baculovirus expression vectors. Nat Biotechnol. 14:1288-1292.
37. Jarvis DL, Fleming JA, Kovacs GR, Summers MD, Guarino LA. 1990. Use of early baculovirus promoters for continuous expression and efficient processing of foreign gene products in stably transformed lepidopteran cells. Nat Biotechnol. 8:950-955.
38. Jarvis DL, Howe D, Aumiller JJ. 2001. Novel baculovirus expression vectors that provide sialylation of recombinant glycoproteins in lepidopteran insect cells. J Virol. 75:6223-6227.
39. Jarvis DL, Weinkauf C, Guarino LA. 1996. Immediate-early baculovirus vectors for foreign gene expression in transformed or infected insect cells. Prot Expr Purif. 8:191-203.
40. Jefferis R. 2009. Glycosylation as a strategy to improve antibody-based therapeutics. Nat Rev Drug Discov. 8:226-234.
41. Kaba SA, Salcedo AM, Wafula PO, Vlak JM, van OMM. 2004. Development of a chitinase and v-cathepsin negative bacmid for improved integrity of secreted recombinant proteins. J Virol. Methods. 122:113-118.
42. Kanda Y, Imai-Nishiya H, Kuni-Kamochi R, Mori K, Inoue M, Kitajima-Miyama K, Okazaki A, Iida S, Shitara K, Satoh M. 2007. Establishment of a GDP-mannose 4,6-dehydratase (GMD) knockout host cell line: A new strategy for generating completely non-fucosylated recombinant therapeutics. J Biotechnol. 130:300-310.
43. King TP, Sobotka AK, Kochoumian L, Lichtenstein LM. 1976. Allergens of honey bee venom. Arch Biochem Biophys. 172:661-671.
44. Kitts PA, Possee RD. 1993. A method for producing recombinant baculovirus expression vectors at high frequency. Biotechniques. 14:810-817.
45. Kost TA, Ignar DM, Clay WC, Andrews J, Leray JD, Overton L, Hoffman CR, Kilpatrick KE, Ellis B, Emerson DL. 1997. Production of a urokinase plasminogen activator-IgG fusion protein (uPA-IgG) in the baculovirus expression system. Gene. 190:139-144.
46. Krammer F, Schinko T, Palmberger D, Tauer C, Messner P, Grabherr R. 2010. Trichoplusia ni cells (High Five) are highly efficient for the production of influenza A virus-like particles: A comparison of two insect cell lines as production platforms for influenza vaccines. Mol Biotechnol. 45:226-234.
47. Kubelka V, Altmann F, Marz L. 1995. The asparagine-linked carbohydrate of honeybee venom hyaluronidase. Glycoconj J. 12:77-83.
48. Kwon HJ, Abi-Mosleh L, Wang ML, Deisenhofer J, Goldstein JL, Brown MS, Infante RE. 2009. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell. 137:1213-1224.
49. Li C, Rossomando A, Wu SL, Karger BL. 2013. Comparability analysis of anti-CD20 commercial (rituximab) and RNAi-mediated fucosylated antibodies by two LC-MS approaches. MAbs. 5:565-575.
50. Lim SH, Beers SA, French RR, Johnson PW, Glennie MJ, Cragg MS. 2010. Anti-CD20 monoclonal antibodies: Historical and future perspectives. Haematologica. 95:135-143.
51. Mabashi-Asazuma H, Shi X, Geisler C, Kuo CW, Khoo KH, Jarvis DL. 2013. Impact of a human CMP-sialic acid transporter on recombinant glycoprotein sialylation in glycoengineered insect cells. Glycobiology. 23:199-210.
52. Maeda S. 1989. Gene transfer vectors of a baculovirus, Bombyx mori nuclear polyhedrosis virus, and their use for expression of foreign genes in insect cells. In: Mitsuhashi J, editor. Invertebrate Cell System Applications, vol. I. Boca Raton, FL: CRC Press. p. 167-181.
53. Malphettes L, Freyvert Y, Chang J, Liu PQ, Chan E, Miller JC, Zhou Z, Nguyen T, Tsai C, Snowden AW, et al. 2010. Highly efficient deletion of FUT8 in CHO cell lines using zinc-finger nucleases yields cells that produce completely nonfucosylated antibodies. Biotechnol Bioeng. 106:774-783.
54. Marchal I, Jarvis DL, Cacan R, Verbert A. 2001. Glycoproteins from insect cells: Sialylated or not? Biol Chem. 382:151-159.
55. Merchant M, Ma X, Maun HR, Zheng Z, Peng J, Romero M, Huang A, Yang NY, Nishimura M, Greve J, et al. 2013. Monovalent antibody design and mechanism of action of onartuzumab, a MET antagonist with anti-tumor activity as a therapeutic agent. Proc Natl Acad Sci USA. 110: E2987-E2996.
56. Ngantung FA, Miller PG, Brushett FR, Tang GL,Wang DI. 2006. RNA interference of sialidase improves glycoprotein sialic acid content consistency. Biotechnol Bioeng. 95:106-119.
57. Okada T, Ihara H, Ito R, Nakano M, Matsumoto K, Yamaguchi Y, Taniguchi N, Ikeda Y. 2010. N-Glycosylation engineering of lepidopteran insect cells by the introduction of the β1,4-N-acetylglucosaminyltransferase III gene. Glycobiology. 20:1147-1159.
58. Owen C, Stewart DA. 2012. Obinutuzumab for the treatment of lymphoproliferative disorders. Exp Op Biol Ther. 12:343-351.
59. Palmberger D, Rendic D, Tauber P, Krammer F, Wilson IB, Grabherr R. 2011. Insect cells for antibody production: Evaluation of an efficient alternative. J Biotechnol. 153:160-166.
60. Palmberger D, Wilson IB, Berger I, Grabherr R, Rendic D. 2012. SweetBac: A new approach for the production of mammalianised glycoproteins in insect cells. PLoS One. 7:e34226.
61. Paschinger K, Staudacher E, Stemmer U, Fabini G, Wilson IB. 2005. Fucosyltransferase substrate specificity and the order of fucosylation in invertebrates. Glycobiology. 15:463-474.
62. Passarelli AL, Guarino LA. 2007. Baculovirus late and very late gene regulation. Curr Drug Targets. 8:1103-1115.
63. Prenner C, Mach L, Glossl J, Marz L. 1992. The antigenicity of the carbohydrate moiety of an insect glycoprotein, honey-bee (Apis mellifera) venom phospholipase A2. The role of α1,3-fucosylation of the asparagine-bound N-acetylglucosamine. Biochem J. 284:377-380.
64. Rankl NB, Rice JW, Gurganus TM, Barbee JL, Burns DJ. 1994. The production of an active protein kinase C-delta in insect cells is greatly enhanced by the use of the basic protein promoter. Prot Expr Purif. 5:346-356.
65. Rendi? D, Klaudiny J, Stemmer U, Schmidt J, Paschinger K, Wilson IB. 2007. Towards abolition of immunogenic structures in insect cells: Characterization of a honey-bee (Apis mellifera) multi-gene family reveals both an allergy-related core α1,3-fucosyltransferase and the first insect Lewis-histo-blood-group-related antigen-synthesizing enzyme. Biochem J. 402:105-115.
66. Rhomberg S, Fuchsluger C, Rendic D, Paschinger K, Jantsch V, Kosma P, Wilson IB. 2006. Reconstitution in vitro of the GDP-fucose biosynthetic pathways of Caenorhabditis elegans and Drosophila melanogaster. FEBS J. 273:2244-2256.
67. Rocchetta HL, Pacan JC, Lam JS. 1998. Synthesis of the A-band polysaccharide sugar D-rhamnose requires Rmd and WbpW: Identification of multiple AlgA homologues, WbpW and ORF488, in Pseudomonas aeruginosa. Mol Microbiol. 29:1419-1434.
68. Rudd PM, Downing AK, Cadene M, Harvey DJ, Wormald MR, Weir I, Dwek RA, Rifkin DB, Gleizes PE. 2000. 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. 39:1596-1603.
69. Satoh M, Iida S, Shitara K. 2006. Non-fucosylated therapeutic antibodies as next-generation therapeutic antibodies. Exp Opin Biol Ther. 6:1161-1173.
70. Savary AC, Georges B, Auriault C. 1999. Adaptation of BTI-TN5B1-4 (high five) insect cells for large-scale production in a stirred bioreactor. Biotechniques. 27:448-450.
71. Seismann H, Blank S, Braren I, Greunke K, Cifuentes L, Grunwald T, Bredehorst R, Ollert M, Spillner E. 2010. Dissecting cross-reactivity in hymenoptera venom allergy by circumvention of α-1,3-core fucosylation. Mol Immunol. 47:799-808.
72. Seo NS, Hollister JR, Jarvis DL. 2001. Mammalian glycosyltransferase expression allows sialoglycoprotein production by baculovirus-infected insect cells. Prot Expr Purif. 22:234-241.
73. Shi X, Harrison RL, Hollister JR, Mohammed A, Fraser MJJ, Jarvis DL. 2007. Construction and characterization of new piggyBac vectors for constitutive or inducible expression of heterologous gene pairs and the identification of a previously unrecognized activator sequence in piggyBac. BMC Biotechnol. 7:5.
74. Shields RL, Lai J, Keck R, O'Connell LY, Hong K, Meng YG, Weikert SH, Presta LG. 2002. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcγRIII and antibody-dependent cellular toxicity. J Biol Chem. 277:26733-26740.
75. Shinkawa T, Nakamura K, Yamane N, Shoji-Hosaka E, Kanda Y, Sakurada M, Uchida K, Anazawa H, Satoh M, Yamasaki M, et al. 2003. The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J Biol Chem. 278:3466-3473.
76. Slack JM, Kuzio J, Faulkner P. 1995. Characterization of v-cath, a cathepsin L-like proteinase expressed by the baculovirus Autographa californica multiple nuclear polyhedrosis virus. J Gen Virol. 76:1091-1098.
77. Sokolenko S, George S, Wagner A, Tuladhar A, Andrich JM, Aucoin MG. 2012. Co-expression vs. co-infection using baculovirus expression vectors in insect cell culture: Benefits and drawbacks. Biotechnol Adv. 30:766-781.
78. Sridhar P, Panda AK, Pal R, Talwar GP, Hasnain SE. 1993. Temporal nature of the promoter and not relative strength determines the expression of an extensively processed protein in a baculovirus system. FEBS Lett. 315:282-286.
79. Summers MD, Smith GE. 1987. A Manual of Methods for Baculovirus Vectors and Insect Cell Culture Procedures. Tx Ag Expt Stn Bull No 1555, Texas Agricultural Experiment Station, College Station, Texas.
80. Taticek RA, McKenna KA, Granados RR, Shuler ML. 1997. Rapid initiation of suspension cultures of Trichoplusia ni insect cells (TN 5B-1-4) using heparin. Biotechnol Tech. 11:237-240.
81. Tomiya N, Howe D, Aumiller JJ, Pathak M, Park J, Palter KB, Jarvis DL, Betenbaugh MJ, Lee YC. 2003. Complex-type biantennary N-glycans of recombinant human transferrin from Trichoplusia ni insect cells expressing mammalian β-1,4-galactosyltransferase and β-1,2-N-acetylglucosaminyltransferase II. Glycobiology. 13:23-34.
82. Toth AM, Geisler C, Aumiller JJ, Jarvis DL. 2011. Factors affecting recombinant Western equine encephalitis virus glycoprotein production in the baculovirus system. Prot Expr Purif. 80:274-282.
83. Tretter V, Altmann F, Marz L. 1991. Peptide-N4-(N-acetyl-β- glucosaminyl)asparagine amidase F cannot release glycans with fucose attached α1→3 to the asparagine-linked N-acetylglucosamine residue. Eur J Biochem. 199:647-652.
84. Usami A, Suzuki T, Nagaya H, Kaki H, Ishiyama S. 2010. Silkworm as a host of baculovirus expression. Curr Pharm Biotechnol. 11:246-250.
85. Varki A, Gagneux P. 2012. Multifarious roles of sialic acids in immunity. Ann N Y Acad Sci. 1253:16-36.
86. von Horsten HH, Ogorek C, Blanchard V, Demmler C, Giese C, Winkler K, Kaup M, Berger M, Jordan I, Sandig V. 2010. Production of non-fucosylated antibodies by co-expression of heterologous GDP-6-deoxy-D-lyxo-4-hexulose reductase. Glycobiology. 20:1607-1618.
87. Wagner R, Liedtke S, Kretzschmar E, Geyer H, Geyer R, Klenk HD. 1996. Elongation of the N-glycans of fowl plague virus hemagglutinin expressed in Spodoptera frugiperda (Sf9) cells by coexpression of human β1,2-N- acetylglucosaminyltransferase I. Glycobiology. 6:165-175.
88. Wickham TJ, Davis T, Granados RR, Shuler ML, Wood HA. 1992. Screening of insect cell lines for the production of recombinant proteins and infectious virus in the baculovirus expression system. Biotechnol Progr. 8:391-396.
89. Yamane-Ohnuki N, Kinoshita S, Inoue-Urakubo M, Kusunoki M, Iida S, Nakano R, Wakitani M, Niwa R, Sakurada M, Uchida K, et al. 2004. Establishment of FUT8 knockout Chinese hamster ovary cells: An ideal host cell line for producing completely defucosylated antibodies with enhanced antibody-dependent cellular cytotoxicity. Biotechnol Bioeng. 87:614-622.
90. Yamane-Ohnuki N, Satoh M. 2009. Production of therapeutic antibodies with controlled fucosylation. MAbs. 1:230-236.
91. Yun EY, Goo TW, Kim SW, Choi KH, Hwang JS, Kang SW, Kwon OY. 2005. Galatosylation and sialylation of mammalian glycoproteins produced by baculovirus-madiated gene expression in insect cells. Biotechnol Lett. 27:1035-1039.
92. Zhong X, Cooley C, Seth N, Juo ZS, Presman E, Resendes N, Kumar R, Allen M, Mosyak L, Stahl M, et al. 2012. Engineering novel Lec1 glycosylation mutants in CHO-DUKX cells: Molecular insights and effector modulation of N-acetylglucosaminyltransferase I. Biotechnol Bioeng. 109:1723-1734.