Lepidopteran cells: An alternative for the production of recombinant antibodies?

mAbs

Volumn 4, Issue 3, 2012, Pages 294-309

  Cérutti, Martine ^a   Golay, Josée ^b  

^a CNRS GDR3260   (France)

^b OSPEDALI RIUNITI   (Italy)

Author keywords

Antibody derived molecules; Baculovirus; Glycosylation; Insect cells; Recombinant antibody; Therapeutic antibodies

Indexed keywords

IMMUNOGLOBULIN E ANTIBODY; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G1 ANTIBODY; MONOCLONAL ANTIBODY; RECOMBINANT ANTIBODY;

ANIMAL CELL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; BACULOVIRUS; COMPLEMENT DEPENDENT CYTOTOXICITY; COST; HOST RANGE; HUMAN; INSECT CELL; LEPIDOPTERA; NONHUMAN; PROTEIN GLYCOSYLATION; REVIEW; VERTEBRATE; VIRUS RECOMBINANT;

ANIMALS; ANTIBODIES, MONOCLONAL; BACULOVIRIDAE; COST-BENEFIT ANALYSIS; GENE TRANSFER TECHNIQUES; GLYCOSYLATION; HUMANS; LEPIDOPTERA; RECOMBINANT PROTEINS;

EID: 84860906466     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.4161/mabs.19942     Document Type: Review

References (150)

1. Smith GE, Summers MD, Fraser MJ. Production of human beta interferon in insect cells infected with a baculovirus expression vector. Mol Cell Biol 1983; 3:2156-65; PMID:6318086.
2. Hasemann CA, Capra JD. High-level production of a functional immunoglobulin heterodimer in a baculovirus expression system. Proc Natl Acad Sci USA 1990; 87:3942-6; PMID:2111022; http://dx.doi.org/10.1073/pnas.87.10. 3942.
3. zu Putlitz J, Kubasek WL, Duchêne M, Marget M, von Specht BU, Domdey H. Antibody production in baculovirus-infected insect cells. Biotechnology (NY) 1990; 8:651-4; PMID:1367456; http://dx.doi.org/10.1038/ nbt0790-651.
4. Ayres MD, Howard SC, Kuzio J, Lopez-Ferber M, Possee RD. The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. Virology 1994; 202:586-605; PMID:8030224; http://dx.doi.org/10.1006/viro.1994.1380.
5. Miller LK. Baculoviruses as gene expression vectors. Annu Rev Microbiol 1988; 42:177-99; PMID:3059993; http://dx.doi.org/10.1146/annurev.mi.42.100188. 001141.
6. Kitts PA, Possee RD. A method for producing recombinant baculovirus expression vectors at high frequency. Biotechniques 1993; 14:810-7; PMID:8512707.
7. Luckow VA, Lee SC, Barry GF, Olins PO. Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J Virol 1993; 67:4566-79; PMID:8392598.
8. Noad RJ, Stewart M, Boyce M, Celma CC, Willison KR, Roy P. Multigene expression of protein complexes by iterative modification of genomic Bacmid DNA. BMC Mol Biol 2009; 10:87-99; PMID:19725957; http://dx.doi.org/10.1186/1471- 2199-10-87.
9. Sokolenko S, George S, Wagner A, Tuladhar A, Andrich JM, Aucoin MG. Co-expression vs. co-infection using baculovirus expression vectors in insect cell culture: Benefits and drawbacks. Biotechnol Adv 2012; 30:766-81; PMID:22297133; http://dx.doi.org/10.1016/j.biotechadv.2012.01.009.
10. Poul MA, Cérutti M, Chaabihi H, Devauchelle G, Kaczorek M, Lefranc MP. Design of cassette baculovirus vectors for the production of therapeutic antibodies in insect cells. Immunotechnology 1995; 1:189-96; PMID:9373347; http://dx.doi.org/10.1016/1380-2933(95)00019-4.
11. Liang M, Dübel S, Li D, Queitsch I, Li W, Bautz EKF. Baculovirus expression cassette vectors for rapid production of complete human IgG from phage display selected antibody fragments. J Immunol Methods 2001; 247:119-30; PMID:11150543; http://dx.doi.org/10.1016/S0022-1759(00)00322-7.
12. Kamita SG, Maeda S, Hammock BD. High-frequency homologous recombination between baculoviruses involves DNA replication. J Virol 2003; 77:13053-61; PMID:14645562; http://dx.doi.org/10.1128/JVI.77.24.13053-61.2003.
13. Crouch EA, Passarelli AL. Genetic requirements for homologous recombination in Autographa californica nucleopolyhedrovirus. J Virol 2002; 76:9323-34; PMID:12186915; http://dx.doi.org/10.1128/JVI.76.18.9323-34.2002.
14. Mikhailov VS, Okano K, Rohrmann GF. Baculovirus alkaline nuclease possesses a 5′→3′ exonuclease activity and associates with the DNA-binding protein LEF-3. J Virol 2003; 77:2436-44; PMID:12551981; http://dx.doi.org/10.1128/JVI.77.4.2436-44.2003.
15. Roelvink PW, van Meer MMM, de Kort CAD, Possee RD, Hammock BD, Vlak JM. Dissimilar expression of Autographa californica multiple nucleocapsid nuclear polyhedrosis virus polyhedrin and p10 genes. J Gen Virol 1992; 73:1481-9; PMID:1607866; http://dx.doi.org/10.1099/0022-1317-73-6-1481.
16. Chaabihi H, Ogliastro MH, Martin M, Giraud C, Devauchelle G, Cérutti M. Competition between baculovirus polyhedrin and p10 gene expression during infection of insect cells. J Virol 1993; 67:2664-71; PMID:8474166.
17. 1 domain controls the assembly and secretion of IgG antibodies. Mol Cell 2009; 34:569-79; PMID:19524537; http://dx.doi.org/10.1016/j.molcel.2009.04.028.
18. Furuta T, Ogawa T, Katsuda T, Fujii I, Yamaji H. Efficient production of an antibody Fab fragment using the baculovirus-insect cell system. J Biosci Bioeng 2010; 110:577-81; PMID:20591732; http://dx.doi.org/10.1016/j.jbiosc.2010. 06.001.
19. Hashimoto Y, Zhang S, Blissard GW. Ao38, a new cell line from eggs of the black witch moth, Ascalapha odorata (Lepidoptera: Noctuidae), is permissive for AcMNPV infection and produces high levels of recombinant proteins. BMC Biotechnol 2010; 10:50-65; PMID:20602790; http://dx.doi.org/10.1186/1472-6750- 10-50.
20. Hancock K, Narang S, Pattabhi S, Yushak ML, Khan A, Lin SC, et al. False positive reactivity of recombinant, diagnostic, glycoproteins produced in High Five insect cells: effect of glycosylation. J Immunol Methods 2008; 330:130-6; PMID:17868684; http://dx.doi.org/10.1016/j.jim.2007.08.002.
21. + antibody. VH and VL junctional diversity are essential for binding activity. J Biol Chem 1991; 266:7626-32; PMID:2019590.
22. Hasemann CA, Capra JD. Mutational analysis of the cross-reactive idiotype of the A strain mouse. J Immunol 1991; 147:3170-9; PMID:1717589.
23. Nesbit M, Fu ZF, McDonald-Smith J, Steplewski Z, Curtis PJ. Production of a functional monoclonal antibody recognizing human colorectal carcinoma cells from a baculovirus expression system. J Immunol Methods 1992; 151:201-8; PMID:1629610; http://dx.doi.org/10.1016/0022-1759(92)90118-D.
24. Hsu TA, Eiden JJ, Bourgarel P, Meo T, Betenbaugh MJ. Effects of co-expressing chaperone BiP on functional antibody production in the baculovirus system. Protein Expr Purif 1994; 5:595-603; PMID:7858430; http://dx.doi.org/10. 1006/prep.1994.1082.
25. Ailor E, Betenbaugh MJ. Overexpression of a cytosolic chaperone to improve solubility and secretion of a recombinant IgG protein in insect cells. Biotechnol Bioeng 1998; 58:196-203; PMID:10191390; http://dx.doi.org/10.1002/ (SICI)1097-0290(19980420)58:2/3<196::AIDBIT12>3.0.CO;2-B.
26. Poul MA, Cérutti M, Chaabihi H, Ticchioni M, Deramoudt FX, Bernard A, et al. Cassette baculovirus vectors for the production of chimeric, humanized or human antibodies in insect cells. Eur J Immunol 1995; 25:2005-9; PMID:7542600; http://dx.doi.org/10.1002/eji.1830250731.
27. Hu P, Glasky MS, Yun A, Alauddin MM, Hornick JL, Khawli LA, et al. A human-mouse chimeric Lym-1 monoclonal antibody with specificity for human lymphomas expressed in a baculovirus system. Hum Antibodies Hybridomas 1995; 6:57-67; PMID:7492752.
28. Troadec S, Bès C, Chentouf M, Nguyen B, Briant L, Jacquet C, et al. Biological activities on T lymphocytes of a baculovirus-expressed chimeric recombinant IgG1 antibody with specificity for the CDR3-like loop on the D1 domain of the CD4 molecule. Clin Immunol 2006; 119:38-50; PMID:16426893; http://dx.doi.org/10.1016/j.clim.2005.11.013.
29. Huang YX, Han J, Dong CF, Sun L, Gao C, Wang XF, et al. Generation of genetic engineering monoclonal antibodies against prion protein. Med Microbiol Immunol 2007; 196:241-6; PMID:17486363; http://dx.doi.org/10.1007/s00430-007- 0049-y.
30. Jar AM, Osorio FA, López OJ. Mouse x pig chimeric antibodies expressed in Baculovirus retain the same properties of their parent antibodies. Biotechnol Prog 2009; 25:516-23; PMID:19301248; http://dx.doi.org/10.1002/btpr. 113.
31. Edelman L, Margaritte C, Chaabihi H, Monchâtre E, Blanchard D, Cardona A, et al. Obtaining a functional recombinant anti-rhesus (D) antibody using the baculovirus-insect cell expression system. Immunology 1997; 91:13-9; PMID:9203960; http://dx.doi.org/10.1046/j.1365-2567.1997.00219.x.
32. Lieby P, Soley A, Levallois H, Hugel B, Freyssinet JM, Cérutti M, et al. The clonal analysis of anticardiolipin antibodies in a single patient with primary antiphospholipid syndrome reveals an extreme antibody heterogeneity. Blood 2001; 97:3820-8; PMID:11389022; http://dx.doi.org/10.1182/ blood.V97.12.3820.
33. Lieby P, Soley A, Knapp AM, Cérutti M, Freyssinet JM, Pasquali JL, et al. Memory B cells producing somatically mutated antiphospholipid antibodies are present in healthy individuals. Blood 2003; 102:2459-65; PMID:12791657; http://dx.doi.org/10.1182/blood-2003-01-0180.
34. 2 protein. Virology 2003; 308:64-73; PMID:12706090; http://dx.doi.org/10.1016/S0042-6822(02)00094-6.
35. 1 protein and definition of the neutralizing domain. J Med Virol 2003; 69:99-107; PMID:12436484; http://dx.doi.org/10.1002/jmv.10259.
36. Lieby P, Poindron V, Roussi S, Klein C, Knapp AM, Garaud JC, et al. Pathogenic antiphospholipid antibody: an antigen-selected needle in a haystack. Blood 2004; 104:1711-5; PMID:15166038; http://dx.doi.org/10.1182/blood-2004-02- 0462.
37. Duan T, Wang XF, Xiao SY, Gu SY, Liang MF. Recombinant human IgG antibodies against human cytomegalovirus. Biomed Environ Sci 2008; 21:372-80; PMID:19133610; http://dx.doi.org/10.1016/S0895-3988(08)60057-4.
38. Sun L, Lu X, Li C, Wang M, Liu Q, Li Z, et al. Generation, characterization and epitope mapping of two neutralizing and protective human recombinant antibodies against influenza A H5N1 viruses. PLoS One 2009; 4:5476; PMID:19421326; http://dx.doi.org/10.1371/journal.pone.0005476.
39. Thurner L, Müller A, Cérutti M, Martin T, Pasquali JL, Gross WL, et al. Wegener's granuloma harbors B lymphocytes with specificities against a proinflammatory transmembrane protein and a tetraspanin. J Autoimmun 2011; 36:87-90; PMID:20951001; http://dx.doi.org/10.1016/j.jaut.2010.09.002.
40. Carayannopoulos L, Max EE, Capra JD. Recombinant human IgA expressed in insect cells. Proc Natl Acad Sci USA 1994; 91:8348-52; PMID:8078886; http://dx.doi.org/10.1073/pnas.91.18.8348.
41. Potter KN, Li Y, Mageed RA, Jefferis R, Capra JD. Anti-idiotypic antibody D12 and superantigen SPA both interact with human VH3-encoded antibodies on the external face of the heavy chain involving FR1, CDR2 and FR3. Mol Immunol 1998; 35:1179-87; PMID:10199392; http://dx.doi.org/10.1016/S0161-5890(98)00103-5.
42. Fukushima N, Nalbandian G, Van De Water J, White K, Ansari AA, Leung P, et al. Characterization of recombinant monoclonal IgA anti-PDC-E2 autoantibodies derived from patients with PBC. Hepatology 2002; 36:1383-92; PMID:12447863.
43. Vangelista L, Laffer S, Turek R, Grönlund H, Sperr WR, Valent P, et al. The immunoglobulin-like modules Cepsilon3 and α2 are the minimal units necessary for human IgE-FcepsilonRI interaction. J Clin Invest 1999; 103:1571-8; PMID:10359566; http://dx.doi.org/10.1172/JCI6551.
44. Björklund JEM, Schmidt M, Magnusson CGM. Characterisation of recombinant human IgE-Fc fragments expressed in baculovirus-infected insect cells. Mol Immunol 2000; 37:169-77; PMID:10865116; http://dx.doi.org/10.1016/ S0161-5890(00)00028-6.
45. Vernersson M, Pejler G, Kristersson T, Alving K, Hellman L. Cloning, structural analysis and expression of the pig IgEε chain. Immunogenetics 1997; 46:461-8; PMID:9321425; http://dx.doi.org/10.1007/s002510050306.
46. Rindisbacher L, Cottet S, Wittek R, Kraehenbuhl JP, Corthésy B. Production of human secretory component with dimeric IgA binding capacity using viral expression systems. J Biol Chem 1995; 270:14220-8; PMID:7775483; http://dx.doi.org/10.1074/jbc.270.23.14220.
47. Laroche Y, Demaeyer M, Stassen JM, Gansemans Y, Demarsin E, Matthyssens G, et al. Characterization of a recombinant single-chain molecule comprising the variable domains of a monoclonal antibody specific for human fibrin fragment D-dimer. J Biol Chem 1991; 266:16343-9; PMID:1885569.
48. Kretzschmar T, Aoustin L, Zingel O, Marangi M, Vonach B, Towbin H, et al. High-level expression in insect cells and purification of secreted monomeric single-chain Fv antibodies. J Immunol Methods 1996; 195:93-101; PMID:8814324; http://dx.doi.org/10.1016/0022-1759(96)00093-2.
49. Lemeulle C, Chardès T, Montavon C, Chaabihi H, Mani JC, Pugnière M, et al. Anti-digoxin scFv fragments expressed in bacteria and in insect cells have different antigen binding properties. FEBS Lett 1998; 423:159-66; PMID:9512350; http://dx.doi.org/10.1016/S0014-5793(98)00029-5.
50. Demangel C, Zhou J, Choo ABH, Shoebridge G, Halliday GM, Britton WJ. Single chain antibody fragments for the selective targeting of antigens to dendritic cells. Mol Immunol 2005; 42:979-85; PMID:15829289; http://dx.doi.org/10.1016/j.molimm.2004.09.034.
51. Yoshida S, Kobayashi T, Matsuoka H, Seki C, Gosnell WL, Chang SP, et al. T-cell activation and cytokine production via a bispecific single-chain antibody fragment targeted to blood-stage malaria parasites. Blood 2003; 101:2300-6; PMID:12411309; http://dx.doi.org/10.1182/blood-2002-03-0831.
52. 3. J Biol Chem 1994; 269:18781-8; PMID:7518445.
53. Bès C, Cérutti M, Briant-Longuet L, Bresson D, Peraldi-Roux S, Pugnière M, et al. The chimeric mouse-human anti-CD4 Fab 13B8.2 expressed in baculovirus inhibits both antigen presentation and HIV-1 promoter activation. Hum Antibodies 2001; 10:67-76; PMID:11673661.
54. Yamaji H, Manabe T, Watakabe K, Muraoka M, Fujii I, Fukuda H. Production of functional antibody Fab fragment by recombinant insect cells. Biochem Eng J 2008; 41:203-9; http://dx.doi.org/10.1016/j.bej.2008.04.017.
55. Johnson GA, Hansen TR, Austin KJ, Van Kirk EA, Murdoch WJ. Baculovirus-insect cell production of bioactive choriogonadotropin- immunoglobulin G heavy-chain fusion proteins in sheep. Biol Reprod 1995; 52:68-73; PMID:7711185; http://dx.doi.org/10.1095/biolreprod52.1.68.
56. Bei R, Schlom J, Kashmiri SVS. Baculovirus expression of a functional single-chain immunoglobulin and its IL-2 fusion protein. J Immunol Methods 1995; 186:245-55; PMID:7594624; http://dx.doi.org/10.1016/0022-1759(95)00149-5.
57. Hu P, Hornick JL, Glasky MS, Yun A, Milkie MN, Khawli LA, et al. A chimeric Lym-1/interleukin 2 fusion protein for increasing tumor vascular permeability and enhancing antibody uptake. Cancer Res 1996; 56:4998-5004; PMID:8895756.
58. Muraki M, Honda S. Efficient production of human Fas receptor extracellular domain-human IgG1 heavy chain Fc domain fusion protein using baculovirus/silkworm expression system. Protein Expr Purif 2010; 73:209-16; PMID:20576530; http://dx.doi.org/10.1016/j.pep.2010.05.007.
59. Maeda S, Kawai T, Obinata M, Fujiwara H, Horiuchi T, Saeki Y, et al. Production of human α-interferon in silkworm using a baculovirus vector. Nature 1985; 315:592-4; PMID:2989694; http://dx.doi.org/10.1038/315592a0.
60. Reis U, Blum B, von Specht BU, Domdey H, Collins J. Antibody production in silkworm cells and silkworm larvae infected with a dual recombinant Bombyx mori nuclear polyhedrosis virus. Biotechnology (NY) 1992; 10:910-2; PMID:1368987; http://dx.doi.org/10.1038/nbt0892-910.
61. Sakamoto S, Pongkitwitoon B, Nakamura S, Maenaka K, Tanaka H, Morimoto S. Efficient silkworm expression of single-chain variable fragment antibody against ginsenoside Re using Bombyx mori nucleopolyhedrovirus bacmid DNA system and its application in enzyme-linked immunosorbent assay for quality control of total ginsenosides. J Biochem 2010; 148:335-40; PMID:20592135; http://dx.doi.org/10.1093/jb/mvq072.
62. Park EY, Ishikiriyama M, Nishina T, Kato T, Yagi H, Kato K, et al. Human IgG1 expression in silkworm larval hemolymph using BmNPV bacmids and its N-linked glycan structure. J Biotechnol 2009; 139:108-14; PMID:18984019; http://dx.doi.org/10.1016/j.jbiotec.2008.09.013.
63. Dojima T, Nishina T, Kato T, Uno T, Yagi H, Kato K, et al. Improved secretion of molecular chaperone-assisted human IgG in silkworm, and no alterations in their N-linked glycan structures. Biotechnol Prog 2010; 26:232-8; PMID:19918885.
64. O'Connell KP, Kovaleva E, Campbell JH, Anderson PE, Brown SG, Davis DC, et al. Production of a recombinant antibody fragment in whole insect larvae. Mol Biotechnol 2007; 36:44-51; PMID:17827537; http://dx.doi.org/10.1007/s12033-007- 0014-4.
65. McCarroll L, King LA. Stable insect cell cultures for recombinant protein production. Curr Opin Biotechnol 1997; 8:590-4; PMID:9353223; http://dx.doi.org/10.1016/S0958-1669(97)80034-1.
66. Farrell PJ, Behie LA, Iatrou K. Transformed Lepidopteran insect cells: new sources of recombinant human tissue plasminogen activator. Biotechnol Bioeng 1999; 64:426-33; PMID:10397881; http://dx.doi.org/10.1002/(SICI)1097- 0290(19990820)64:4<426::AID-BIT5>3.0.CO;2-#.
67. Tessier DC, Thomas DY, Khouri HE, Laliberté F, Vernet T. Enhanced secretion from insect cells of a foreign protein fused to the honeybee melittin signal peptide. Gene 1991; 98:177-83; PMID:2016060; http://dx.doi.org/10.1016/ 0378-1119(91)90171-7.
68. Yokoyama N, Hirata M, Ohtsuka K, Nishiyama Y, Fujii K, Fujita M, et al. Co-expression of human chaperone Hsp70 and Hsdj or Hsp40 co-factor increases solubility of overexpressed target proteins in insect cells. Biochim Biophys Acta 2000; 1493:119-24; PMID:10978513.
69. Nakajima M, Kato T, Kanamasa S, Park EY. Molecular chaperone-assisted production of human α-1,4-N-acetylglucosaminyltransferase in silkworm larvae using recombinant BmNPV bacmids. Mol Biotechnol 2009; 43:67-75; PMID:19418270; http://dx.doi.org/10.1007/s12033-009-9174-8.
70. Feige MJ, Hendershot LM, Buchner J. How antibodies fold. Trends Biochem Sci 2010; 35:189-98; PMID:20022755; http://dx.doi.org/10.1016/j.tibs.2009.11. 005.
71. Douris V, Swevers L, Labropoulou V, Andronopoulou E, Georgoussi Z, Iatrou K. Stably transformed insect cell lines: tools for expression of secreted and membrane-anchored proteins and high-throughput screening platforms for drug and insecticide discovery. Adv Virus Res 2006; 68:113-56; PMID:16997011; http://dx.doi.org/10.1016/S0065-3527(06)68004-4.
72. 2-protein in stably-transformed insect cells. J Immunol Methods 2000; 246:97-108; PMID:11121551; http://dx.doi.org/10.1016/S0022-1759(00)00299-4.
73. Guttieri MC, Sinha T, Bookwalter C, Liang M, Schmaljohn CS. Cassette vectors for conversion of Fab fragments into full-length human IgG1 monoclonal antibodies by expression in stably transformed insect cells. Hybrid Hybridomics 2003; 22:135-45; PMID:12954098; http://dx.doi.org/10.1089/153685903322286548.
74. 2-specific, neutralizing IgG monoclonal antibody to Puumala virus. Virology 1997; 235:252-60; PMID:9281505; http://dx.doi.org/10.1006/viro. 1997.8695.
75. Shields RL, Lai J, Keck R, O'Connell LY, Hong K, Meng YG, et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 2002; 277:26733-40; PMID:11986321; http://dx.doi.org/10.1074/jbc.M202069200.
76. Marchal I, Mir AM, Kmiécik D, Verbert A, Cacan R. Use of inhibitors to characterize intermediates in the processing of N-glycans synthesized by insect cells: a metabolic study with Sf9 cell line. Glycobiology 1999; 9:645-54; PMID:10362833; http://dx.doi.org/10.1093/glycob/9.7.645.
77. Altmann F, Kornfeld G, Dalik T, Staudacher E, Glössl J. Processing of asparagine-linked oligosaccharides in insect cells. N- acetylglucosaminyltransferase I and II activities in cultured lepidopteran cells. Glycobiology 1993; 3:619-25; PMID:8130393; http://dx.doi.org/10.1093/ glycob/3.6.619.
78. Lopez M, Coddeville B, Langridge J, Lemoine J, Plancke H, Chaabihi H, et al. Microheterogeneity of the oligosaccharides carried by the N-glycosylation sites of the bovine lactotransferrin expressed in Mamestra brassicae using a baculovirus vector. Glycobiology 1997; 7:635-51; PMID:9254046; http://dx.doi.org/10.1093/glycob/7.5.635.
79. Altmann F, Schwihla H, Staudacher E, Glössl J, März L. Insect cells contain an unusual, membrane-bound beta-N-acetylglucosaminidase probably involved in the processing of protein N-glycans. J Biol Chem 1995; 270:17344-9; PMID:7615537; http://dx.doi.org/10.1074/jbc.270.29.17344.
80. Staudacher E, Kubelka V, März L. Distinct N-glycan fucosylation potentials of three lepidopteran cell lines. Eur J Biochem 1992; 207:987-93; PMID:1499571; http://dx.doi.org/10.1111/j.1432-033.1992.tb17134.x.
81. Prenner C, Mach L, Glössl J, März L. The antigenicity of the carbohydrate moiety of an insect glycoprotein, honey-bee (Apis mellifera) venom phospholipase A2. The role of alpha1,3-fucosylation of the asparagine-bound N-acetylglucosamine. Biochem J 1992; 284:377-80; PMID:1376112.
82. Song M, Park DY, Kim Y, Lee KJ, Lu Z, Ko K, et al. Characterization of N-glycan structures and biofunction of anti-colorectal cancer monoclonal antibody CO17-1A produced in baculovirus-insect cell expression system. J Biosci Bioeng 2010; 110:135-40; PMID:20547339; http://dx.doi.org/10.1016/j.jbiosc. 2010.01.013.
83. Aumiller JJ, Mabashi-Asazuma H, Hillar A, Shi X, Jarvis DL. A new glycoengineered insect cell line with an inducibly mammalianized protein N-glycosylation pathway. Glycobiology 2012; 22:417-28; PMID:22042767; http://dx.doi.org/10.1093/glycob/cwr160.
84. Wagner R, Liedtke S, Kretzschmar E, Geyer H, Geyer R, Klenk HD. Elongation of the N-glycans of fowl plague virus hemagglutinin expressed in Spodoptera frugiperda (Sf9) cells by coexpression of human beta 1,2-N-acetylglucosaminyltransferase I. Glycobiology 1996; 6:165-75; PMID:8727789; http://dx.doi.org/10.1093/glycob/6.2.165.
85. Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 2002; 99:754-8; PMID:11806974; http://dx.doi.org/10.1182/blood.V99.3.754.
86. Niwa R, Natsume A, Uehara A, Wakitani M, Iida S, Uchida K, et al. IgG subclass-independent improvement of antibody-dependent cellular cytotoxicity by fucose removal from Asn297-linked oligosaccharides. J Immunol Methods 2005; 306:151-60; PMID:16219319; http://dx.doi.org/10.1016/j.jim.2005.08.009.
87. Niwa R, Shoji-Hosaka E, Sakurada M, Shinkawa T, Uchida K, Nakamura K, et al. Defucosylated chimeric anti-CC chemokine receptor 4 IgG1 with enhanced antibody-dependent cellular cytotoxicity shows potent therapeutic activity to T-cell leukemia and lymphoma. Cancer Res 2004; 64:2127-33; PMID:15026353; http://dx.doi.org/10.1158/0008-5472.CAN-03-2068.
88. Junttila TT, Parsons K, Olsson C, Lu Y, Xin Y, Theriault J, et al. Superior in vivo efficacy of afucosylated trastuzumab in the treatment of HER2-amplified breast cancer. Cancer Res 2010; 70:4481-9; PMID:20484044; http://dx.doi.org/10.1158/0008-5472.CAN-09-3704.
89. Herbst R, Wang Y, Gallagher S, Mittereder N, Kuta E, Damschroder M, et al. B-cell depletion in vitro and in vivo with an afucosylated anti-CD19 antibody. J Pharmacol Exp Ther 2010; 335:213-22; PMID:20605905; http://dx.doi.org/10.1124/jpet.110.168062.
90. Ferrara C, Grau S, Jäger C, Sondermann P, Brünker P, Waldhauer I, et al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Natl Acad Sci USA 2011; 108:12669-74; PMID:21768335; http://dx.doi.org/10.1073/ pnas.1108455108.
91. Jefferis R. Recombinant antibody therapeutics: the impact of glycosylation on mechanisms of action. Trends Pharmacol Sci 2009; 30:356-62; PMID:19552968; http://dx.doi.org/10.1016/j.tips.2009.04.007.
92. Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol 2007; 25:21-50; PMID:17029568; http://dx.doi.org/10.1146/ annurev.immunol.25.022106.141702.
93. Iizuka M, Ogawa S, Takeuchi A, Nakakita S, Kubo Y, Miyawaki Y, et al. Production of a recombinant mouse monoclonal antibody in transgenic silkworm cocoons. FEBS J 2009; 276:5806-20; PMID:19740109; http://dx.doi.org/10.1111/j. 1742-4658.2009.07262.x.
94. Cragg MS, Morgan SM, Chan HT, Morgan BP, Filatov AV, Johnson PW, et al. Complement-mediated lysis by anti-CD20 mAb correlates with segregation into lipid rafts. Blood 2003; 101:1045-52; PMID:12393541; http://dx.doi.org/10.1182/ blood-2002-06-1761.
95. Raju TS. Terminal sugars of Fc glycans influence antibody effector functions of IgGs. Curr Opin Immunol 2008; 20:471-8; PMID:18606225; http://dx.doi.org/10.1016/j.coi.2008.06.007.
96. Wright A, Morrison SL. Effect of C2-associated carbohydrate structure on Ig effector function: studies with chimeric mouse-human IgG1 antibodies in glycosylation mutants of Chinese hamster ovary cells. J Immunol 1998; 160:3393-402; PMID:9531299.
97. Hodoniczky J, Zheng YZ, James DC. Control of recombinant monoclonal antibody effector functions by Fc N-glycan remodeling in vitro. Biotechnol Prog 2005; 21:1644-52; PMID:16321047; http://dx.doi.org/10.1021/bp050228w.
98. Raju ST. Impact of Fc glycosylation on monoclonal antibody effector functions and degradation by proteases. Current Trends in Monoclonal Antibody Development and Manufacturing Biotechnology: Pharmaceutical Aspects. Edited by Shire SJ, Gombotz W, Bechtold-Peters K, Andya J. New-York: Springer 2010; 11:249-69.
99. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 2008; 8:34-47; PMID:18064051; http://dx.doi.org/10. 1038/nri2206.
100. Troadec S, Chentouf M, Cérutti M, Nguyen B, Olive D, Bès C, et al. In vitro antitumoral activity of baculovirus-expressed chimeric recombinant anti-CD4 antibody 13B8.2 on T-cell lymphomas. J Immunother 2007; 30:190-202; PMID:17471166; http://dx.doi.org/10.1097/01.cji.0000211331.61019.26.
101. Swanson JA, Hoppe AD. The coordination of signaling during Fc receptor-mediated phagocytosis. J Leukoc Biol 2004; 76:1093-103; PMID:15466916; http://dx.doi.org/10.1189/jlb.0804439.
102. Bologna L, Gotti E, Manganini M, Rambaldi A, Intermesoli T, Introna M, et al. Mechanism of action of type II, glycoengineered, anti-CD20 monoclonal antibody GA101 in B-chronic lymphocytic leukemia whole blood assays in comparison with rituximab and alemtuzumab. J Immunol 2011; 186:3762-9; PMID:21296976; http://dx.doi.org/10.4049/jimmunol.1000303.
103. Ashraf SQ, Umana P, Mössner E, Ntouroupi T, Brünker P, Schmidt C, et al. Humanised IgG1 antibody variants targeting membrane-bound carcinoembryonic antigen by antibody-dependent cellular cytotoxicity and phagocytosis. Br J Cancer 2009; 101:1758-68; PMID:19904275; http://dx.doi.org/ 10.1038/sj.bjc.6605355.
104. Birch JR, Racher AJ. Antibody production. Adv Drug Deliv Rev 2006; 58:671-85; PMID:16822577; http://dx.doi.org/10.1016/j.addr.2005.12.006.
105. Jefferis R. Glycosylation as a strategy to improve antibody-based therapeutics. Nat Rev Drug Discov 2009; 8:226-34; PMID:19247305; http://dx.doi.org/10.1038/nrd2804.
106. Olivier S, Jacoby M, Brillon C, Bouletreau S, Mollet T, Nerriere O, et al. EB66 cell line, a duck embryonic stem cell-derived substrate for the industrial production of therapeutic monoclonal antibodies with enhanced ADCC activity. MAbs 2010; 2:405-15; PMID:20562528.
107. Arnold DF, Misbah SA. Cetuximab-induced anaphylaxis and IgE specific for galactose-alpha-1,3-galactose. N Engl J Med 2008; 358:2735, author reply 2735-6; PMID:18565869; http://dx.doi.org/10.1056/NEJMc080834.
108. Hossler P, Khattak SF, Li ZJ. Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology 2009; 19:936-49; PMID:19494347; http://dx.doi.org/10.1093/glycob/cwp079.
109. Kaern M, Elston TC, Blake WJ, Collins JJ. Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 2005; 6:451-64; PMID:15883588; http://dx.doi.org/10.1038/nrg1615.
110. Pilbrough W, Munro TP, Gray P. Intraclonal protein expression heterogeneity in recombinant CHO cells. PLoS One 2009; 4:8432; PMID:20037651; http://dx.doi.org/10.1371/journal.pone.0008432.
111. Geisse S. reflections on more than 10 years of TGE (Transient Gene Expression) approaches. Protein Expr Purif 2009; 64:99-107; PMID:19027070; http://dx.doi.org/10.1016/j.pep.2008.10.017.
112. Wood CR, Boss MA, Kenten JH, Calvert JE, Roberts NA, Emtage JS. The synthesis and in vivo assembly of functional antibodies in yeast. Nature 1985; 314:446-9; PMID:3920532; http://dx.doi.org/10.1038/314446a0.
113. Horwitz AH, Chang CP, Better M, Hellstrom KE, Robinson RR. Secretion of functional antibody and Fab fragment from yeast cells. Proc Natl Acad Sci USA 1988; 85:8678-82; PMID:3054890; http://dx.doi.org/10.1073/pnas.85.22.8678.
114. Rakestraw JA, Sazinsky SL, Piatesi A, Antipov E, Wittrup KD. Directed evolution of a secretory leader for the improved expression of heterologous proteins and full-length antibodies in Saccharomyces cerevisiae. Biotechnol Bioeng 2009; 103:1192-201; PMID:19459139; http://dx.doi.org/10.1002/bit.22338.
115. Evans L, Hughes M, Waters J, Cameron J, Dodsworth N, Tooth D, et al. The production, characterisation and enhanced pharmacokinetics of scFv-albumin fusions expressed in Saccharomyces cerevisiae. Protein Expr Purif 2010; 73:113-24; PMID:20546898; http://dx.doi.org/10.1016/j.pep.2010.05.009.
116. Jacobs PP, Geysens S, Vervecken W, Contreras R, Callewaert N. Engineering complextype N-glycosylation in Pichia pastoris using GlycoSwitch technology. Nat Protoc 2009; 4:58-70; PMID:19131957; http://dx.doi.org/10.1038/nprot.2008. 213.
117. Kuroda K, Kobayashi K, Kitagawa Y, Nakagawa T, Tsumura H, Komeda T, et al. Efficient antibody production upon suppression of O mannosylation in the yeast Ogataea minuta. Appl Environ Microbiol 2008; 74:446-53; PMID:18039826; http://dx.doi.org/10.1128/AEM.02106-07.
118. Choi BK, Bobrowicz P, Davidson RC, Hamilton SR, Kung DH, Li H, et al. Use of combinatorial genetic libraries to humanize N-linked glycosylation in the yeast Pichia pastoris. Proc Natl Acad Sci USA 2003; 100:5022-7; PMID:12702754; http://dx.doi.org/10.1073/pnas.0931263100.
119. Hamilton SR, Bobrowicz P, Bobrowicz B, Davidson RC, Li H, Mitchell T, et al. Production of complex human glycoproteins in yeast. Science 2003; 301:1244-6; PMID:12947202; http://dx.doi.org/10.1126/science.1088166.
120. Bobrowicz P, Davidson RC, Li H, Potgieter TI, Nett JH, Hamilton SR, et al. Engineering of an artificial glycosylation pathway blocked in core oligosaccharide assembly in the yeast Pichia pastoris: production of complex humanized glycoproteins with terminal galactose. Glycobiology 2004; 14:757-66; PMID:15190003; http://dx.doi.org/10.1093/glycob/cwh104.
121. Hamilton SR, Gerngross TU. Glycosylation engineering in yeast: the advent of fully humanized yeast. Curr Opin Biotechnol 2007; 18:387-92; PMID:17951046; http://dx.doi.org/10.1016/j.copbio.2007.09.001.
122. Rahbarizadeh F, Rasaee MJ, Forouzandeh M, Allameh AA. Overexpression of anti-MUC1 single-domain antibody fragments in the yeast Pichia pastoris. Mol Immunol 2006; 43:426-35; PMID:16337485; http://dx.doi.org/10.1016/j.molimm.2005. 03.003.
123. Li H, Sethuraman N, Stadheim TA, Zha D, Prinz B, Ballew N, et al. Optimization of humanized IgGs in glycoengineered Pichia pastoris. Nat Biotechnol 2006; 24:210-5; PMID:16429149; http://dx.doi.org/10.1038/nbt1178.
124. Ward M, Lin C, Victoria DC, Fox BP, Fox JA, Wong DL, et al. Characterization of humanized antibodies secreted by Aspergillus niger. Appl Environ Microbiol 2004; 70:2567-76; PMID:15128505; http://dx.doi.org/10.1128/ AEM.70.5.2567-76.2004.
125. Nyyssönen E, Penttilä M, Harkki A, Saloheimo A, Knowles JKC, Keränen S. Efficient production of antibody fragments by the filamentous fungus Trichoderma reesei. Biotechnology (NY) 1993; 11:591-5; PMID:7763606; http://dx.doi.org/10.1038/nbt0593-591.
126. Wallis GLF, Easton RL, Jolly K, Hemming FW, Peberdy JF. Galactofuranoic-oligomannose N-linked glycans of α-galactosidase A from Aspergillus niger. Eur J Biochem 2001; 268:4134-43; PMID:11488905; http://dx.doi.org/10.1046/j.1432-327.2001.02322.x.
127. Hiatt A, Cafferkey R, Bowdish K. Production of antibodies in transgenic plants. Nature 1989; 342:76-8; PMID:2509938; http://dx.doi.org/10.1038/342076a0.
128. Peters J, Stoger E. Transgenic crops for the production of recombinant vaccines and anti-microbial antibodies. Hum Vaccin 2011; 7:367-74; PMID:21346415; http://dx.doi.org/10.4161/hv.7.3.14303.
129. Komarova TV, Baschieri S, Donini M, Marusic C, Benvenuto E, Dorokhov YL. Transient expression systems for plant-derived biopharmaceuticals. Expert Rev Vaccines 2010; 9:859-76; PMID:20673010; http://dx.doi.org/10.1586/erv.10.85.
130. Pogue GP, Vojdani F, Palmer KE, Hiatt E, Hume S, Phelps J, et al. Production of pharmaceutical-grade recombinant aprotinin and a monoclonal antibody product using plant-based transient expression systems. Plant Biotechnol J 2010; 8:638-54; PMID:20514694; http://dx.doi.org/10.1111/j.1467- 7652.2009.00495.x.
131. Giritch A, Marillonnet S, Engler C, van Eldik G, Botterman J, Klimyuk V, et al. Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc Natl Acad Sci USA 2006; 103:14701-6; PMID:16973752; http://dx.doi.org/10.1073/pnas.0606631103.
132. Huang Z, Phoolcharoen W, Lai H, Piensook K, Cardineau G, Zeitlin L, et al. High-level rapid production of full-size monoclonal antibodies in plants by a single-vector DNA replicon system. Biotechnol Bioeng 2010; 106:9-17; PMID:20047189.
133. Cabanes-Macheteau M, Fitchette-Lainé AC, Loutelier-Bourhis C, Lange C, Vine ND, Ma JK, et al. N-Glycosylation of a mouse IgG expressed in transgenic tobacco plants. Glycobiology 1999; 9:365-72; PMID:10089210; http://dx.doi.org/10.1093/glycob/9.4.365.
134. Schähs M, Strasser R, Stadlmann J, Kunert R, Rademacher T, Steinkellner H. Production of a monoclonal antibody in plants with a humanized N-glycosylation pattern. Plant Biotechnol J 2007; 5:657-63; PMID:17678502; http://dx.doi.org/10.1111/j.1467-7652.2007.00273.x.
135. Bakker H, Bardor M, Molthoff JW, Gomord V, Elbers I, Stevens LH, et al. Galactose-extended glycans of antibodies produced by transgenic plants. Proc Natl Acad Sci USA 2001; 98:2899-904; PMID:11226338; http://dx.doi.org/10.1073/ pnas.031419998
136. Paccalet T, Bardor M, Rihouey C, Delmas F, Chevalier C, D'Aoust MA, et al. Engineering of a sialic acid synthesis pathway in transgenic plants by expression of bacterial Neu5Ac-synthesizing enzymes. Plant Biotechnol J 2007; 5:16-25; PMID:17207253; http://dx.doi.org/10.1111/j.1467-7652.2006.00211.x.
137. Gasdaska J, Spencer D, Dickey L. Advantages of therapeutic protein production in the aquatic plant lemna. Bioprocess J 2003; 2:49-56.
138. Cox KM, Sterling JD, Regan JT, Gasdaska JR, Frantz KK, Peele CG, et al. Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat Biotechnol 2006; 24:1591-7; PMID:17128273; http://dx.doi.org/10.1038/ nbt1260.
139. Koprivova A, Stemmer C, Altmann F, Hoffmann A, Kopriva S, Gorr G, et al. Targeted knockouts of Physcomitrella lacking plant-specific immunogenic N-glycans. Plant Biotechnol J 2004; 2:517-23; PMID:17147624; http://dx.doi.org/10.1111/j.1467-7652.2004.00100.x.
140. Tran M, Zhou B, Pettersson PL, Gonzalez MJ, Mayfield SP. Synthesis and assembly of a full-length human monoclonal antibody in algal chloroplasts. Biotechnol Bioeng 2009; 104:663-73; PMID:19562731.
141. Specht E, Miyake-Stoner S, Mayfield S. Micro-algae come of age as a platform for recombinant protein production. Biotechnol Lett 2010; 32:1373-83; PMID:20556634; http://dx.doi.org/10.1007/s10529-010-0326-5.
142. Boss MA, Kenten JH, Wood CR, Emtage JS. Assembly of functional antibodies from immunoglobulin heavy and light chains synthesised in E. coli. Nucleic Acids Res 1984; 12:3791-806; PMID:6328437; http://dx.doi.org/10.1093/nar/12.9. 3791.
143. Cabilly S, Riggs AD, Pande H, Shively JE, Holmes WE, Rey M, et al. Generation of antibody activity from immunoglobulin polypeptide chains produced in Escherichia coli. Proc Natl Acad Sci USA 1984; 81:3273-7; PMID:6374653; http://dx.doi.org/10.1073/pnas.81.11.3273.
144. Simmons LC, Reilly D, Klimowski L, Raju TS, Meng G, Sims P, et al. Expression of full-length immunoglobulins in Escherichia coli: rapid and efficient production of aglycosylated antibodies. J Immunol Methods 2002; 263:133-47; PMID:12009210; http://dx.doi.org/10.1016/S0022-1759(02)00036-4.
145. Reilly DE, Yansura DG. Production of monoclonal antibodies in E. coli. In current trends in monoclonal antibody development and manufacturing. Edited by Shire SJ, Gombotz W, Bechtold-Peters K, Andya J. New-York: Springer 2010; 295-308.
146. Raju TS, Scallon BJ. Glycosylation in the Fc domain of IgG increases resistance to proteolytic cleavage by papain. Biochem Biophys Res Commun 2006; 341:797-803; PMID:16442075; http://dx.doi.org/10.1016/j.bbrc.2006.01.030.
147. 1 variants productively engage activating Fc receptors. Proc Natl Acad Sci USA 2008; 105:20167-72; PMID:19074274; http://dx.doi.org/10.1073/pnas.0809257105.
148. Jung ST, Kang TH, Kelton W, Georgiou G. Bypassing glycosylation: engineering aglycosylated full-length IgG antibodies for human therapy. Curr Opin Biotechnol 2011; 22:858-67; PMID:21420850; http://dx.doi.org/10.1016/j. copbio.2011.03.002.
149. Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P. Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Biol 2003; 325:979-89; PMID:12527303; http://dx.doi.org/10.1016/S0022-2836(02)01250-0.
150. Mena JA, Kamen AA. Insect cell technology is a versatile and robust vaccine manufacturing platform. Expert Rev Vaccines 2011; 10:1063-81; PMID:21806400; http://dx.doi.org/10.1586/erv.11.24.