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Humanizing glycosylation pathways in eukaryotic expression systems

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Abstract

Glycosylation represents the most widespread posttranslational modifications, found in a broad spectrum of natural and therapeutic recombinant proteins. It highly affects bioactivity, site-specificity, stability, solubility, immunogenicity, and serum half-life of glycoproteins. Numerous expression hosts including yeasts, insect cells, transgenic plants, and mammalian cells have been explored for synthesizing therapeutic glycoproteins. However, glycosylation profile of eukaryotic expression systems differs from human. Glycosylation strategies have been proposed for humanizing the glycosylation pathways in expression hosts which is the main theme of this review. Besides, we also highlighted the glycosylation potential of protozoan parasites by emphasizing on the mammalian-like glycosylation potential of Leishmania tarentolae known as Leishmania expression system.

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References

  • Ablain J, Durand Ellen M, Yang S, Zhou Y, Zon Leonard I (2015) A CRISPR/Cas9 vector system for tissue-specific gene disruption in zebrafish. Dev Cell 32:756–764. doi:10.1016/j.devcel.2015.01.032

    Article  CAS  Google Scholar 

  • Alexandrov K, Grün M (2001) Protein expression systems for non-pathogenic Kinetoplastidae. Google Patents CA2388151 A1

  • Anyaogu DC, Mortensen UH (2015) Manipulating the glycosylation pathway in bacterial and lower eukaryotes for production of therapeutic proteins. Curr Opin Biotechnol 36:122–128

    Article  CAS  Google Scholar 

  • Aoki-Kinoshita KF (2013) Using databases and web resources for glycomics research. Mol Cell Proteomics 12:1036–1045

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Baghban R, Gargari SLM, Rajabibazl M, Nazarian S, Bakherad H (2016) Camelid-derived heavy-chain nanobody against Clostridium botulinum neurotoxin E in Pichia pastoris. Biotechnol Appl Biochem 63:200–205

    Article  CAS  Google Scholar 

  • Bazl MR et al (2007) Production of chimeric recombinant single domain antibody-green fluorescent fusion protein in Chinese hamster ovary cells. Hybridoma 26:1–9

    Article  CAS  Google Scholar 

  • Böhm E et al (2015) Differences in N-glycosylation of recombinant human coagulation factor VII derived from BHK, CHO, and HEK293 cells. BMC Biotechnol 15:1

    Article  CAS  Google Scholar 

  • Bosques CJ et al (2010) Chinese hamster ovary cells can produce galactose-[alpha]-1, 3-galactose antigens on proteins. Nat Biotechnol 28:1153–1156

    Article  CAS  Google Scholar 

  • Breitling R et al (2002) Non-pathogenic trypanosomatid protozoa as a platform for protein research and production. Protein Expr Purif 25:209–218

    Article  CAS  Google Scholar 

  • Breton C, Fournel-Gigleux S, Palcic MM (2012) Recent structures, evolution and mechanisms of glycosyltransferases. Curr Opin Struct Biol 22:540–549

    Article  CAS  Google Scholar 

  • Castilho A, Steinkellner H (2012) Glyco-engineering in plants to produce human-like N-glycan structures. Biotechnol J 7:1088–1098

    Article  CAS  Google Scholar 

  • Castilho A et al (2010) In planta protein sialylation through overexpression of the respective mammalian pathway. J Biol Chem 285:15923–15930

    Article  CAS  Google Scholar 

  • Castilho A et al (2011) N-glycosylation engineering of plants for the biosynthesis of glycoproteins with bisected and branched complex N-glycans. Glycobiology 21:813–823

    Article  CAS  Google Scholar 

  • Chen C-Y, Lin C-Y, Chen G-Y, Hu Y-C (2011) Baculovirus as a gene delivery vector: recent understandings of molecular alterations in transduced cells and latest applications. Biotechnol Adv 29:618–631

    Article  CAS  Google Scholar 

  • Chen L, Yang X, Yuan H, Zhu L, Yue W (2014) [Construction and investigation of a recombinant eukaryotic expression vector for expressing the ORF3 protein of hepatitis E virus in BHK-21 fibroblasts]. Zhonghua gan zang bing za zhi = Zhonghua ganzangbing zazhi = Chinese J Hepatol 22:499–503

    CAS  Google Scholar 

  • Cheon SA, Kim H, Oh D-B, Kwon O, Kang HA (2012) Remodeling of the glycosylation pathway in the methylotrophic yeast Hansenula polymorpha to produce human hybrid-type N-glycans. J Microbiol 50:341–348

    Article  CAS  Google Scholar 

  • Choi B-K et al (2012) Improvement of N-glycan site occupancy of therapeutic glycoproteins produced in Pichia pastoris. Appl Microbiol Biotechnol 95:671–682

    Article  CAS  Google Scholar 

  • Chung CH et al (2008) Cetuximab-induced anaphylaxis and IgE specific for galactose-α-1, 3-galactose. N Engl J Med 358:1109–1117

    Article  CAS  Google Scholar 

  • Cox KM et al (2006) Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat Biotechnol 24:1591–1597

    Article  CAS  Google Scholar 

  • Czarnota A, Tyborowska J, Peszyńska-Sularz G, Gromadzka B, Bieńkowska-Szewczyk K, Grzyb K (2016) Immunogenicity of Leishmania-derived hepatitis B small surface antigen particles exposing highly conserved E2 epitope of hepatitis C virus. Microb Cell Fact 15:1

    Article  Google Scholar 

  • Dalziel M, Crispin M, Scanlan CN, Zitzmann N, Dwek RA (2014) Emerging principles for the therapeutic exploitation of glycosylation. Science 343:1235681

    Article  CAS  Google Scholar 

  • Damasceno LM, Huang C-J, Batt CA (2012) Protein secretion in Pichia pastoris and advances in protein production. Appl Microbiol Biotechnol 93:31–39

    Article  CAS  Google Scholar 

  • Davies J, Jiang L, Pan LZ, LaBarre MJ, Anderson D, Reff M (2001) Expression of GnTIII in a recombinant anti-CD20 CHO production cell line: expression of antibodies with altered glycoforms leads to an increase in ADCC through higher affinity for FCγRIII. Biotechnol Bioeng 74:288–294

    Article  CAS  Google Scholar 

  • Dean N (1999) Asparagine-linked glycosylation in the yeast Golgi. Biochim Biophys Acta (BBA)-Gen Subj 1426:309–322

    Article  CAS  Google Scholar 

  • DiCarlo JE, Norville JE, Mali P, Rios X, Aach J, Church GM (2013) Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 41:4336–4343

    Article  CAS  Google Scholar 

  • Faye L, Boulaflous A, Benchabane M, Gomord V, Michaud D (2005) Protein modifications in the plant secretory pathway: current status and practical implications in molecular pharming. Vaccine 23:1770–1778

    Article  CAS  Google Scholar 

  • Ferrara C, Brünker P, Suter T, Moser S, Püntener U, Umaña P (2006) Modulation of therapeutic antibody effector functions by glycosylation engineering: influence of Golgi enzyme localization domain and co-expression of heterologous β1, 4-N-acetylglucosaminyltransferase III and Golgi α-mannosidase II. Biotechnol Bioeng 93:851–861

    Article  CAS  Google Scholar 

  • Fujiyama K, Furukawa A, Katsura A, Misaki R, Omasa T, Seki T (2007) Production of mouse monoclonal antibody with galactose-extended sugar chain by suspension cultured tobacco BY2 cells expressing human β (1, 4)-galactosyltransferase. Biochem Biophys Res Commun 358:85–91

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Geisler C, Aumiller JJ, Jarvis DL (2008) A fused lobes gene encodes the processing β-N-acetylglucosaminidase in Sf9 cells. J Biol Chem 283:11330–11339

    Article  CAS  Google Scholar 

  • Ghaderi D, Taylor RE, Padler-Karavani V, Diaz S, Varki A (2010) Implications of the presence of N-glycolylneuraminic acid in recombinant therapeutic glycoproteins. Nat Biotechnol 28:863–867

    Article  CAS  Google Scholar 

  • Gomord V, Faye L (2004) Posttranslational modification of therapeutic proteins in plants. Curr Opin Plant Biol 7:171–181

    Article  CAS  Google Scholar 

  • Gomord V, Chamberlain P, Jefferis R, Faye L (2005) Biopharmaceutical production in plants: problems, solutions and opportunities. Trends Biotechnol 23:559–565

    Article  CAS  Google Scholar 

  • Haile S, Papadopoulou B (2007) Developmental regulation of gene expression in trypanosomatid parasitic protozoa. Curr Opin Microbiol 10:569–577

    Article  CAS  Google Scholar 

  • Hamilton SR et al (2006) Humanization of yeast to produce complex terminally sialylated glycoproteins. Science 313:1441–1443

    Article  CAS  Google Scholar 

  • Harrison RL, Jarvis DL (2006) Protein N-glycosylation in the baculovirus-insect cell expression system and engineering of insect cells to produce “mammalianized” recombinant glycoproteins. Adv Virus Res 68:159–191

    Article  CAS  Google Scholar 

  • Hashimoto K et al (2006) KEGG as a glycome informatics resource. Glycobiology 16:63R–70R

    Article  CAS  Google Scholar 

  • He T, Xu S, Zhang G, Nakanishi H, Gao X (2014) [Reconstruction of N-glycosylation pathway for producing human glycoproteins in Saccharomyces cerevisiae]. Wei sheng wu xue bao = Acta Microbiol Sin 54:509–516

    CAS  Google Scholar 

  • Hennet T, Cabalzar J (2015) Congenital disorders of glycosylation: a concise chart of glycocalyx dysfunction. Trends Biochem Sci 40:377–384

    Article  CAS  Google Scholar 

  • Hirabayashi J (2004) Lectin-based structural glycomics: glycoproteomics and glycan profiling. Glycoconj J 21:35–40

    Article  Google Scholar 

  • Hou J, Tyo KE, Liu Z, Petranovic D, Nielsen J (2012) Metabolic engineering of recombinant protein secretion by Saccharomyces cerevisiae. FEMS Yeast Res 12:491–510

    Article  CAS  Google Scholar 

  • Ilgoutz SC, Zawadzki JL, Ralton JE, McConville MJ (1999) Evidence that free GPI glycolipids are essential for growth of Leishmania mexicana. EMBO J 18:2746–2755

    Article  CAS  Google Scholar 

  • Jacobs P, Callewaert N (2009) N-glycosylation engineering of biopharmaceutical expression systems. Curr Mol Med 9:774–800

    Article  CAS  Google Scholar 

  • Jin C, Bencúrová M, Borth N, Ferko B, Jensen-Jarolim E, Altmann F, Hantusch B (2006) Immunoglobulin G specifically binding plant N-glycans with high affinity could be generated in rabbits but not in mice. Glycobiology 16:349–357

    Article  CAS  Google Scholar 

  • Jin C et al (2008) A plant-derived human monoclonal antibody induces an anti-carbohydrate immune response in rabbits. Glycobiology 18:235–241

    Article  CAS  Google Scholar 

  • Kawamura YI et al (2008) DNA hypermethylation contributes to incomplete synthesis of carbohydrate determinants in gastrointestinal cancer. Gastroenterology 135(142–151):e143

    Google Scholar 

  • Khan AH, Sadroddiny E (2015) Licensed monoclonal antibodies and associated challenges. Hum Antibodies 23:63–72. doi:10.3233/HAB-150286

    Article  Google Scholar 

  • Khan AH, Sadroddiny E (2016) Application of immuno-PCR for the detection of early stage cancer. Mol Cell Probes 30:106–112. doi:10.1016/j.mcp.2016.01.010

    Article  CAS  Google Scholar 

  • Kim YK, Kim KR, Kang DG, Jang SY, Kim YH, Cha HJ (2011) Expression of β-1, 4-galactosyltransferase and suppression of β-N-acetylglucosaminidase to aid synthesis of complex N-glycans in insect Drosophila S2 cells. J Biotechnol 153:145–152

    Article  CAS  Google Scholar 

  • Kim NY, Choi HS, Shin SH, Choi JY (2012) Short-hairpin RNA-mediated gene expression interference in Trichoplusia ni cells. J Microbiol Biotechnol 22:190–198

    Article  CAS  Google Scholar 

  • Klatt S, Rohe M, Alagesan K, Kolarich D, Konthur Z, Hartl D (2013) Production of glycosylated soluble amyloid precursor protein alpha (sAPPalpha) in Leishmania tarentolae. J Proteome Res. doi:10.1021/pr300693f

    Google Scholar 

  • Koprivova A et al (2004) Targeted knockouts of Physcomitrella lacking plant-specific immunogenic N-glycans. Plant Biotechnol J 2:517–523

    Article  CAS  Google Scholar 

  • Kost TA, Condreay JP, Jarvis DL (2005) Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nat Biotechnol 23:567–575

    Article  CAS  Google Scholar 

  • Krainer FW et al (2013) Knockout of an endogenous mannosyltransferase increases the homogeneity of glycoproteins produced in Pichia pastoris. Sci Rep 3:3279

    Article  Google Scholar 

  • Kushnir S, Cirstea IC, Basiliya L, Lupilova N, Breitling R, Alexandrov K (2011) Artificial linear episome-based protein expression system for protozoon Leishmania tarentolae. Mol Biochem Parasitol 176:69–79

    Article  CAS  Google Scholar 

  • Lauc G, Zoldoš V (2010) Protein glycosylation: an evolutionary crossroad between genes and environment. Mol BioSyst 6:2373–2379

    Article  CAS  Google Scholar 

  • Lawrence SM et al (2001) Cloning and expression of human sialic acid pathway genes to generate CMP-sialic acids in insect cells. Glycoconj J 18:205–213

    Article  CAS  Google Scholar 

  • Li H, d’Anjou M (2009) Pharmacological significance of glycosylation in therapeutic proteins. Curr Opin Biotechnol 20:678–684

    Article  CAS  Google Scholar 

  • Liang X-H, Haritan A, Uliel S, Michaeli S (2003) Trans and cis splicing in trypanosomatids: mechanism, factors, and regulation. Eukaryot Cell 2:830–840

    Article  CAS  Google Scholar 

  • Lim Y, Wong NS, Lee YY, Ku SC, Wong DC, Yap MG (2010) Engineering mammalian cells in bioprocessing–current achievements and future perspectives. Biotechnol Appl Biochem 55:175–189

    Article  CAS  Google Scholar 

  • Limkul J, Iizuka S, Sato Y, Misaki R, Ohashi T, Ohashi T, Fujiyama K (2016) The production of human glucocerebrosidase in glyco-engineered Nicotiana benthamiana plants. Plant Biotechnol J 14:1682–1694

    Article  CAS  Google Scholar 

  • Lin N, George HJ, Mascarenhas J, Collingwood TN, Kayser KJ, Achtien K (2015a) Method of producing human-like glycosylation pattern using cells deficient in glutamine synthase, CMP-N-acetylneuraminic acid hydroxylase and/or glycoprotein alpha-1, 3-galactosyltransferase. Google Patents US8980583 B2

  • Lin N et al (2015b) Chinese hamster ovary (CHO) host cell engineering to increase sialylation of recombinant therapeutic proteins by modulating sialyltransferase expression. Biotechnol Prog 31:334–346

    Article  CAS  Google Scholar 

  • Luk FC, Johnson TM, Beckers CJ (2008) N-linked glycosylation of proteins in the protozoan parasite Toxoplasma gondii. Mol Biochem Parasitol 157:169–178

    Article  CAS  Google Scholar 

  • Mabashi-Asazuma H, Shi X, Geisler C, Kuo C-W, Khoo K-H, Jarvis DL (2013) Impact of a human CMP-sialic acid transporter on recombinant glycoprotein sialylation in glycoengineered insect cells. Glycobiology 23:199–210

    Article  CAS  Google Scholar 

  • Mabashi-Asazuma H, Kuo C-W, Khoo K-H, Jarvis DL (2014) A novel baculovirus vector for the production of nonfucosylated recombinant glycoproteins in insect cells. Glycobiology 24:325–340

    Article  CAS  Google Scholar 

  • Mabashi-Asazuma H, Kuo C-W, Khoo K-H, Jarvis DL (2015) Modifying an insect cell N-glycan processing pathway using CRISPR-Cas technology. ACS Chem Biol 10:2199–2208

    Article  CAS  Google Scholar 

  • Macher BA, Galili U (2008) The Galα 1, 3Galβ1, 4GlcNAc-R (α-Gal) epitope: a carbohydrate of unique evolution and clinical relevance. Biochim Biophys Acta (BBA)-Gen Subj 1780:75–88

    Article  CAS  Google Scholar 

  • Majors BS, Betenbaugh MJ, Pederson NE, Chiang GG (2008) Enhancement of transient gene expression and culture viability using Chinese hamster ovary cells overexpressing Bcl-xL. Biotechnol Bioeng 101:567–578

    Article  CAS  Google Scholar 

  • Malphettes L 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

    Article  CAS  Google Scholar 

  • Marchal I, Jarvis DL, Cacan R, Verbert A (2001) Glycoproteins from insect cells: sialylated or not? Biol Chem 382:151–159

    Article  CAS  Google Scholar 

  • Naegeli A et al (2014) Molecular analysis of an alternative N-glycosylation machinery by functional transfer from Actinobacillus pleuropneumoniae to Escherichia coli. J Biol Chem 289:2170–2179

    Article  CAS  Google Scholar 

  • Nagasu T et al (1992) Isolation of new temperature-sensitive mutants of Saccharomyces cerevisiae deficient in mannose outer chain elongation. Yeast 8:535–547

    Article  CAS  Google Scholar 

  • Nasab FP, Aebi M, Bernhard G, Frey AD (2013) A combined system for engineering glycosylation efficiency and glycan structure in Saccharomyces cerevisiae. Appl Environ Microbiol 79:997–1007

    Article  CAS  Google Scholar 

  • Nett JH et al (2011) A combinatorial genetic library approach to target heterologous glycosylation enzymes to the endoplasmic reticulum or the Golgi apparatus of Pichia pastoris. Yeast 28:237–252

    Article  CAS  Google Scholar 

  • Niimi T (2012) Recombinant protein production in the eukaryotic protozoan parasite Leishmania tarentolae: a review. Recomb Gene Expr 824:307–315

    Article  CAS  Google Scholar 

  • Onitsuka M et al (2012) Enhancement of sialylation on humanized IgG-like bispecific antibody by overexpression of α2, 6-sialyltransferase derived from Chinese hamster ovary cells. Appl Microbiol Biotechnol 94:69–80

    Article  CAS  Google Scholar 

  • Paccalet T et al (2015) Synthesis of sialic acid in plants. Google Patents

  • Palmberger D, Ashjaei K, Strell S, Hoffmann-Sommergruber K, Grabherr R (2014) Minimizing fucosylation in insect cell-derived glycoproteins reduces binding to IgE antibodies from the sera of patients with allergy. Biotechnol J 9:1206–1214

    Article  CAS  Google Scholar 

  • Park SR et al (2014) Expression, glycosylation and function of recombinant anti-colorectal cancer mAb CO17-1A in SfSWT4 insect cells. Entomol Res 44:39–46

    Article  CAS  Google Scholar 

  • Parodi AJ (1993) N-glycosylation in trypanosomatid protozoa. Glycobiology 3:193–199

    Article  CAS  Google Scholar 

  • Pays E, Nolan DP (1998) Expression and function of surface proteins in Trypanosoma brucei. Mol Biochem Parasitol 91:3–36

    Article  CAS  Google Scholar 

  • Phan H-P, Sugino M, Niimi T (2009) The production of recombinant human laminin-332 in a Leishmania tarentolae expression system. Protein Expr Purif 68:79–84

    Article  CAS  Google Scholar 

  • Piirainen MA, de Ruijter JC, Koskela EV, Frey AD (2014) Glycoengineering of yeasts from the perspective of glycosylation efficiency. New Biotechnol 31:532–537

    Article  CAS  Google Scholar 

  • Pion C et al (2014) Characterization and immunogenicity in mice of recombinant influenza haemagglutinins produced in Leishmania tarentolae. Vaccine 32:5570–5576

    Article  CAS  Google Scholar 

  • Potgieter TI et al (2009) Production of monoclonal antibodies by glycoengineered Pichia pastoris. J Biotechnol 139:318–325. doi:10.1016/j.jbiotec.2008.12.015

    Article  CAS  Google Scholar 

  • Rahimpour A et al (2013) Engineering the cellular protein secretory pathway for enhancement of recombinant tissue plasminogen activator expression in Chinese hamster ovary cells: effects of CERT and XBP1s genes. J Microbiol Biotechnol 23:1116–1122

    Article  CAS  Google Scholar 

  • Rahimpour A, Ahani R, Najaei A, Adeli A, Barkhordari F, Mahboudi F (2016) Development of genetically modified Chinese hamster ovary host cells for the enhancement of recombinant tissue plasminogen activator expression Malaysian. J Med Sci 23:6–13

    Google Scholar 

  • Rahmati M, Khan AH, Razavi S, Khorramizadeh MR, Rasaee MJ, Sadroddiny E (2016) Cloning and expression of human bone morphogenetic protein-2 gene in Leishmania tarentolae. Biocatal Agric Biotechnol 5:199–203. doi:10.1016/j.bcab.2016.01.006

    Google Scholar 

  • Rahmatpour S et al (2016) Application of immuno-PCR assay for the detection of serum IgE specific to Bermuda allergen. Mol Cell Probes. doi:10.1016/j.mcp.2016.10.002

    Google Scholar 

  • Raymond F et al (2011) Genome sequencing of the lizard parasite Leishmania tarentolae reveals loss of genes associated to the intracellular stage of human pathogenic species. Nucleic Acids Res 40:1131–1147

    Article  CAS  Google Scholar 

  • Rich JR, Withers SG (2009) Emerging methods for the production of homogeneous human glycoproteins. Nat Chem Biol 5:206–215

    Article  CAS  Google Scholar 

  • Saint-Jore-Dupas C, Faye L, Gomord V (2007) From planta to pharma with glycosylation in the toolbox. Trends Biotechnol 25:317–323

    Article  CAS  Google Scholar 

  • Samuelson J, Banerjee S, Magnelli P, Cui J, Kelleher DJ, Gilmore R, Robbins PW (2005) The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc Natl Acad Sci USA 102:1548–1553

    Article  CAS  Google Scholar 

  • Schuster M et al (2005) Improved effector functions of a therapeutic monoclonal Lewis Y-specific antibody by glycoform engineering. Cancer Res 65:7934–7941

    CAS  Google Scholar 

  • Schuster M et al (2007) In vivo glyco-engineered antibody with improved lytic potential produced by an innovative non-mammalian expression system. Biotechnol J 2:700–708

    Article  CAS  Google Scholar 

  • Shabani M, Hemmati S, Hadavi R, Amirghofran Z, Jeddi-Tehrani M, Rabbani H, Shokri F (2010) Optimization of gene transfection in murine myeloma cell lines using different transfection reagents. Avicenna J Med Biotechnol 2:123–130

    CAS  Google Scholar 

  • Shin YJ, Chong YJ, Yang MS, Kwon TH (2011) Production of recombinant human granulocyte macrophage-colony stimulating factor in rice cell suspension culture with a human-like N-glycan structure. Plant Biotechnol J 9:1109–1119

    Article  CAS  Google Scholar 

  • Shinkawa T 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

    Article  CAS  Google Scholar 

  • Simpson L, Sbicego S, Aphasizhev R (2003) Uridine insertion/deletion RNA editing in trypanosome mitochondria: a complex business. RNA 9:265–276

    Article  CAS  Google Scholar 

  • Sinclair AM, Elliott S (2005) Glycoengineering: the effect of glycosylation on the properties of therapeutic proteins. J Pharm Sci 94:1626–1635

    Article  CAS  Google Scholar 

  • Smith GE, Summers M, Fraser M (1983) Production of human beta interferon in insect cells infected with a baculovirus expression vector. Mol Cell Biol 3:2156–2165

    Article  CAS  Google Scholar 

  • Stanley P (2011) Golgi glycosylation. Cold Spring Harb Perspect Biol 3:a005199

    Article  CAS  Google Scholar 

  • Struwe WB, Pagel K, Benesch JL, Harvey DJ, Campbell MP (2016) GlycoMob: an ion mobility-mass spectrometry collision cross section database for glycomics. Glycoconj J 33:399–404

    Article  CAS  Google Scholar 

  • Sun T et al (2015) Functional knockout of FUT8 in Chinese hamster ovary cells using CRISPR/Cas9 to produce a defucosylated antibody. Eng Life Sci 15:660–666

    Article  CAS  Google Scholar 

  • Swiech K, Picanço-Castro V, Covas DT (2012) Human cells: new platform for recombinant therapeutic protein production. Protein Expr Purif 84:147–153

    Article  CAS  Google Scholar 

  • Theron CW, Labuschagné M, Gudiminchi R, Albertyn J, Smit MS (2014) A broad-range yeast expression system reveals Arxula adeninivorans expressing a fungal self-sufficient cytochrome P450 monooxygenase as an excellent whole-cell biocatalyst. FEMS Yeast Res 14:556–566

    Article  CAS  Google Scholar 

  • van Oers MM, Pijlman GP, Vlak JM (2015) Thirty years of baculovirus–insect cell protein expression: from dark horse to mainstream technology. J Gen Virol 96:6–23

    Article  CAS  Google Scholar 

  • von Horsten HH et al (2010) Production of non-fucosylated antibodies by co-expression of heterologous GDP-6-deoxy-D-lyxo-4-hexulose reductase. Glycobiology 20:1607–1618

    Article  CAS  Google Scholar 

  • Wildt S, Gerngross TU (2005) The humanization of N-glycosylation pathways in yeast. Nat Rev Microbiol 3:119–128

    Article  CAS  Google Scholar 

  • Xu X et al (2011) The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line. Nat Biotechnol 29:735–741

    Article  CAS  Google Scholar 

  • Xu H, Guo H, Cheung IY, Cheung N-KV (2016) Antitumor efficacy of anti-GD2 IgG1 is enhanced by Fc glyco-engineering. Cancer Immunol Res 4:631–638

    Article  CAS  Google Scholar 

  • Yang Z et al (2015) Engineered CHO cells for production of diverse, homogeneous glycoproteins. Nat Biotechnol 33:842–844

    Article  CAS  Google Scholar 

  • Yin B et al (2015) Glycoengineering of Chinese hamster ovary cells for enhanced erythropoietin N-glycan branching and sialylation. Biotechnol Bioeng 112:2343–2351

    Article  CAS  Google Scholar 

  • Zhu J (2012) Mammalian cell protein expression for biopharmaceutical production. Biotechnol Adv 30:1158–1170

    Article  CAS  Google Scholar 

  • Zoldoš V, Horvat T, Lauc G (2013) Glycomics meets genomics, epigenomics and other high throughput omics for system biology studies. Curr Opin Chem Biol 17:34–40

    Article  CAS  Google Scholar 

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Acknowledgements

This review is the outcome of financially non-supported in house study.

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Authors and Affiliations

  1. Department of Medical Biotechnology, School of Advanced Technologies in Medicine, International Campus, Tehran University of Medical Sciences, Tehran, Iran

    Amjad Hayat Khan

  2. Medical Nano-Technology and Tissue Engineering Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Hadi Bayat & Azam Rahimpour

  3. Department of Tissue Engineering and Regenerative Medicine, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Hadi Bayat & Azam Rahimpour

  4. Department of Clinical Biochemistry, Faculty of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Masoumeh Rajabibazl

  5. Department of Biotechnology, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Masoumeh Rajabibazl

  6. Department of Microbiology, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia (UPM), 43400, Serdang, Selangor, Malaysia

    Suriana Sabri

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Khan, A.H., Bayat, H., Rajabibazl, M. et al. Humanizing glycosylation pathways in eukaryotic expression systems. World J Microbiol Biotechnol 33, 4 (2017). https://doi.org/10.1007/s11274-016-2172-7

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  • DOI: https://doi.org/10.1007/s11274-016-2172-7

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