Protein glycosylation control in mammalian cell culture: Past precedents and contemporary prospects

Advances in Biochemical Engineering/Biotechnology

Volumn 127, Issue , 2012, Pages 187-219

  Hossler, Patrick ^a  

^a ABBOTT LABORATORIES   (United States)

Author keywords

Genomics; Mammalian cell culture; Protein glycosylation; Systems biology

Indexed keywords

PROTEIN;

ANIMAL; ARTICLE; CULTURE TECHNIQUE; GENETICS; GLYCOSYLATION; HUMAN; METABOLISM; METHODOLOGY; PROTEIN PROCESSING;

ANIMALS; CELL CULTURE TECHNIQUES; GLYCOSYLATION; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS;

EID: 84877015785     PISSN: 07246145     EISSN: None     Source Type: Book Series    
DOI: 10.1007/10_2011_113     Document Type: Article

References (115)

1. Apweiler R, Hermjakob H, Sharon N (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim Biophys Acta 1473(1):4-8
2. Walsh MT et al (1990) Effect of the carbohydrate moiety on the secondary structure of beta 2-glycoprotein. I. Implications for the biosynthesis and folding of glycoproteins. Biochemistry 29(26):6250-6257
3. Leavitt R, Schlesinger S, Kornfeld S (1977) Impaired intracellular migration and altered solubility of nonglycosylated glycoproteins of vesicular Stomatitis virus and Sindbis virus. J Biol Chem 252(24):9018-9023
4. Wallick SC, Kabat EA, Morrison SL (1988) Glycosylation of a VH residue of a monoclonal antibody against alpha (1-6) dextran increases its affinity for antigen. J Exp Med 168(3): 1099-109
5. Wyss DF, Wagner G (1996) The structural role of sugars in glycoproteins. Curr Opin Biotechnol 7(4):409-416
6. Butler M (2006) Optimisation of the cellular metabolism of glycosylation for recombinant proteins produced by mammalian cell systems. Cytotechnology 50(1-3):57-76
7. Butler M et al (2003) Detailed glycan analysis of serum glycoproteins of patients with congenital disorders of glycosylation indicates the specific defective glycan processing step and provides an insight into pathogenesis. Glycobiology 13(9):601-622
8. Raman R et al (2005) Glycomics: an integrated systems approach to structure-function relationships of glycans. Nat Methods 2(11):817-824
9. Kikuchi N et al (2005) The carbohydrate sequence markup language (CabosML): an XML description of carbohydrate structures. Bioinformatics 21(8):1717-1718
10. Sahoo SS et al (2005) GLYDE--an expressive XML standard for the representation of glycan structure. Carbohydr Res 340(18):2802-2807
11. Lowe JB, Marth JD (2003) A genetic approach to mammalian glycan function. Annu Rev Biochem 72:643-691
12. Lis H, Sharon N (1993) Protein glycosylation. Structural and functional aspects. Eur J Biochem 218(1):1-27
13. Rudd PM et al (2001) Glycosylation and the immune system. Science 291(5512): 2370-2376
14. Gross V et al (1988) Involvement of various organs in the initial plasma clearance of differently glycosylated rat liver secretory proteins. Eur J Biochem 173(3):653-659
15. Sathyamoorthy N et al (1991) Evidence that specific high mannose structures directly regulate multiple cellular activities. Mol Cell Biochem 102(2):139-147
16. Lifely MR et al (1995) Glycosylation and biological activity of CAMPATH-1H expressed in different cell lines and grown under different culture conditions. Glycobiology 5(8): 813-822
17. Shields RL et al (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 277(30):26733-26740
18. Millward TA et al (2008) Effect of constant and variable domain glycosylation on pharmacokinetics of therapeutic antibodies in mice. Biologicals 36(1):41-47
19. Hossler P, Khattak SF, Li ZJ (2009) Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology 19(9):936-949
20. Helenius A, Aebi M (2001) Intracellular functions of N-linked glycans. Science 291(5512):2364-2369
21. Carraway KL, Hull SR (1989) O-glycosylation pathway for mucin-type glycoproteins. Bioessays 10(4):117-121
22. Van den Steen P et al (1998) Concepts and principles of O-linked glycosylation. Crit Rev Biochem Mol Biol 33(3):151-208
23. Ishida N, Kawakita M (2004) Molecular physiology and pathology of the nucleotide sugar transporter family (SLC35). Pflugers Arch 447(5):768-775
24. Rademacher TW (1993) Glycosylation as a factor affecting product consistency. Biologicals 21(2):103-104
25. Stanley P, Raju TS, Bhaumik M (1996) CHO cells provide access to novel N-glycans and developmentally regulated glycosyltransferases. Glycobiology 6(7):695-699
26. Skibeli V, Nissen-Lie G, Torjesen P (2001) Sugar profiling proves that human serum erythropoietin differs from recombinant human erythropoietin. Blood 98(13):3626-3634
27. Durocher Y, Butler M (2009) Expression systems for therapeutic glycoprotein production. Curr Opin Biotechnol 20(6):700-707
28. Jenkins N, Parekh RB, James DC (1996) Getting the glycosylation right: implications for the biotechnology industry. Nat Biotechnol 14(8):975-981
29. Larsen RD et al (1990) Frameshift and nonsense mutations in a human genomic sequence homologous to a murine UDP-Gal:beta-D-Gal(1, 4)-D-GlcNAc alpha(1, 3)-galactosyltransferase cDNA. J Biol Chem 265(12):7055-7061
30. Baker KN et al (2001) Metabolic control of recombinant protein N-glycan processing in NS0 and CHO cells. Biotechnol Bioeng 73(3):188-202
31. Borys MC et al (2010) Effects of culture conditions on N-glycolylneuraminic acid (Neu5Gc) content of a recombinant fusion protein produced in CHO cells. Biotechnol Bioeng 105(6):1048-1057
32. Lee EU, Roth J, Paulson JC (1989) Alteration of terminal glycosylation sequences on N-linked oligosaccharides of Chinese hamster ovary cells by expression of beta-galactoside alpha 2, 6-sialyltransferase. J Biol Chem 264(23):13848-13855
33. Campbell C, Stanley P (1984) A dominant mutation to ricin resistance in Chinese hamster ovary cells induces UDP-GlcNAc:glycopeptide beta-4-N-acetylglucosaminyltransferase III activity. J Biol Chem 259(21):13370-13378
34. Kim YK et al (2005) Production and N-glycan analysis of secreted human erythropoietin glycoprotein in stably transfected Drosophila S2 cells. Biotechnol Bioeng 92(4):452-461
35. Hamilton SR et al (2006) Humanization of yeast to produce complex terminally sialylated glycoproteins. Science 313(5792):1441-1443
36. Kunkel JP et al (2000) Comparisons of the glycosylation of a monoclonal antibody produced under nominally identical cell culture conditions in two different bioreactors. Biotechnol Prog 16(3):462-470
37. Goldman MH et al (1998) Monitoring recombinant human interferon-gamma N-glycosylation during perfused fluidized-bed and stirred-tank batch culture of CHO cells. Biotechnol Bioeng 60(5):596-607
38. Burger C et al (1999) An integrated strategy for the process development of a recombinant antibody-cytokine fusion protein expressed in BHK cells. Appl Microbiol Biotechnol 52(3):345-353
39. Chotigeat W et al (1994) Role of environmental conditions on the expression levels, glycoform pattern and levels of sialyltransferase for hFSH produced by recombinant CHO cells. Cytotechnology 15(1-3):217-221
40. Lin AA, Kimura R, Miller WM (1993) Production of tPA in recombinant CHO cells under oxygen-limited conditions. Biotechnol Bioeng 42(3):339-350
41. Kunkel JP et al (1998) Dissolved oxygen concentration in serum-free continuous culture affects N-linked glycosylation of a monoclonal antibody. J Biotechnol 62(1):55-71
42. Yoon SK, Song JY, Lee GM (2003) Effect of low culture temperature on specific productivity, transcription level, and heterogeneity of erythropoietin in Chinese hamster ovary cells. Biotechnol Bioeng 82(3):289-298
43. Bollati-Fogolin M et al (2005) Temperature reduction in cultures of hGM-CSF-expressing CHO cells: effect on productivity and product quality. Biotechnol Prog 21(1):17-21
44. Clark KJ, Chaplin FW, Harcum SW (2004) Temperature effects on product-quality-related enzymes in batch CHO cell cultures producing recombinant tPA. Biotechnol Prog 20(6):1888-1892
45. Trummer E et al (2006) Process parameter shifting: part I. Effect of DOT, pH, and temperature on the performance of Epo-Fc expressing CHO cells cultivated in controlled batch bioreactors. Biotechnol Bioeng 94(6):1033-1044
46. Muthing J et al (2003) Effects of buffering conditions and culture pH on production rates and glycosylation of clinical phase I anti-melanoma mouse IgG3 monoclonal antibody R24. Biotechnol Bioeng 83(3):321-334
47. Gramer MJ, Goochee CF (1993) Glycosidase activities in Chinese hamster ovary cell lysate and cell culture supernatant. Biotechnol Prog 9(4):366-373
48. Gramer MJ et al (1995) Removal of sialic acid from a glycoprotein in CHO cell culture supernatant by action of an extracellularCHO cell sialidase. Biotechnology (N Y) 13(7):692-698
49. Gramer MJ, Goochee CF (1994) Glycosidase activities of the 293 and NS0 cell lines, and of an antibody-producing hybridoma cell line. Biotechnol Bioeng 43(5):423-428
50. Thorens B, Vassalli P (1986) Chloroquine and ammonium chloride prevent terminal glycosylation of immunoglobulins in plasma cells without affecting secretion. Nature 321(6070):618-620
51. Andersen DC, Goochee CF (1995) The effect of ammonia on the O-linked glycosylation of granulocyte colony-stimulating factor produced by chinese hamster ovary cells. Biotechnol Bioeng 47(1):96-105
52. Yang M, Butler M (2000) Effects of ammonia on CHO cell growth, erythropoietin production, and glycosylation. Biotechnol Bioeng 68(4):370-380
53. Curling EM et al (1990) Recombinant human interferon-gamma. Differences in glycosylation and proteolytic processing lead to heterogeneity in batch culture. Biochem J 272(2):333-337
54. Borys MC, Linzer DI, Papoutsakis ET (1994) Ammonia affects the glycosylation patterns of recombinant mouse placental lactogen-I by chinese hamster ovary cells in a pH-dependent manner. Biotechnol Bioeng 43(6):505-514
55. Grammatikos SI et al (1998) Intracellular UDP-N-acetylhexosamine pool affects N-glycan complexity: a mechanism of ammonium action on protein glycosylation. Biotechnol Prog 14(3):410-419
56. Hayter PM et al (1992) Glucose-limited chemostat culture of Chinese hamster ovary cells producing recombinant human interferon-gamma. Biotechnol Bioeng 39(3):327-335
57. Hayter PM et al (1993) The effect of the dilution rate on CHO cell physiology and recombinant interferon-gamma production in glucose-limited chemostat culture. Biotechnol Bioeng 42(9):1077-1085
58. Tachibana H et al (1994) Changes of monosaccharide availability of human hybridoma lead to alteration of biological properties of human monoclonal antibody. Cytotechnology 16(3):151-157
59. Cruz HJ et al (2000) Metabolic shifts do not influence the glycosylation patterns of a recombinant fusion protein expressed in BHK cells. Biotechnol Bioeng 69(2):129-139
60. Nyberg GB et al (1999) Metabolic effects on recombinant interferon-gamma glycosylation in continuous culture of Chinese hamster ovary cells. Biotechnol Bioeng 62(3):336-347
61. Crowell CK et al (2007) Amino acid and manganese supplementation modulates the glycosylation state of erythropoietin in a CHO culture system. Biotechnol Bioeng 96(3):538-549
62. Higa HH, Paulson JC (1985) Sialylation of glycoprotein oligosaccharides with N-acetyl-, N-glycolyl-, and N-O-diacetylneuraminic acids. J Biol Chem 260(15):8838-8849
63. Gawlitzek M et al (1995) Characterization of changes in the glycosylation pattern of recombinant proteins from BHK-21 cells due to different culture conditions. J Biotechnol 42(2):117-131
64. Gu X et al (1997) Influence of Primatone RL supplementation on sialylation of recombinant human interferon-gamma produced by Chinese hamster ovary cell culture using serum-free media. Biotechnol Bioeng 56(4):353-360
65. Andersen DC et al (2000) Multiple cell culture factors can affect the glycosylation of Asn-184 in CHO-produced tissue-type plasminogen activator. Biotechnol Bioeng 70(1):25-31
66. Gu X, Wang DI (1998) Improvement of interferon-gamma sialylation in Chinese hamster ovary cell culture by feeding of N-acetylmannosamine. Biotechnol Bioeng 58(6):642-648
67. Wong NS et al (2010) An investigation of intracellular glycosylation activities in CHO cells: effects of nucleotide sugar precursor feeding. Biotechnol Bioeng 107(2):321-336
68. Rosenfeld R et al (2007) A lectin array-based methodology for the analysis of protein glycosylation. J Biochem Biophys Methods 70(3):415-426
69. Lauc G et al (2010) Complex genetic regulation of protein glycosylation. Mol Biosyst 6(2):329-335
70. Ashwell G, Kawasaki T (1978) A protein from mammalian liver that specifically binds galactose-terminated glycoproteins. Methods Enzymol 50:287-288
71. Weikert S et al (1999) Engineering Chinese hamster ovary cells to maximize sialic acid content of recombinant glycoproteins. Nat Biotechnol 17(11):1116-1121
72. Schlenke P et al (1999) Construction and characterization of stably transfected BHK-21 cells with human-type sialylation characteristic. Cytotechnology 30(1-3):17-25
73. Zhang X, Lok SH, Kon OL (1998) Stable expression of human alpha-2, 6-sialyltransferase in Chinese hamster ovary cells: functional consequences for human erythropoietin expression and bioactivity. Biochim Biophys Acta 1425(3):441-452
74. Ferrari J et al (1998) Chinese hamster ovary cells with constitutively expressed sialidase antisense RNA produce recombinant DNase in batch culture with increased sialic acid. Biotechnol Bioeng 60(5):589-595
75. Wong NS, Yap MG, Wang DI (2006) Enhancing recombinant glycoprotein sialylation through CMP-sialic acid transporter over expression in Chinese hamster ovary cells. Biotechnol Bioeng 93(5):1005-1016
76. Chenu S et al (2003) Reduction of CMP-N-acetylneuraminic acid hydroxylase activity in engineered Chinese hamster ovary cells using an antisense-RNA strategy. Biochim Biophys Acta 1622(2):133-144
77. Umana P et al (1999) Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat Biotechnol 17(2):176-180
78. Davies J et al (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 FC gamma RIII. Biotechnol Bioeng 74(4):288-294
79. Mori K et al (2004) Engineering Chinese hamster ovary cells to maximize effector function of produced antibodies using FUT8 siRNA. Biotechnol Bioeng 88(7):901-908
80. Potvin B et al (1990) Transfection of a human alpha-(1, 3)fucosyltransferase gene into Chinese hamster ovary cells. Complications arise from activation of endogenous alpha-(1, 3)fucosyltransferases. J Biol Chem 265(3):1615-1622
81. Yamane-Ohnuki N 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(5):614-622
82. Lim SF et al (2008) The Golgi CMP-sialic acid transporter: a new CHO mutant provides functional insights. Glycobiology 18(11):851-860
83. Chen P, Harcum SW (2006) Effects of elevated ammonium on glycosylation gene expression in CHO cells. Metab Eng 8(2):123-132
84. Oh SK et al (1993) Substantial overproduction of antibodies by applying osmotic pressure and sodium butyrate. Biotechnol Bioeng 42(5):601-610
85. Palermo DP et al (1991) Production of analytical quantities of recombinant proteins in Chinese hamster ovary cells using sodium butyrate to elevate gene expression. J Biotechnol 19(1):35-47
86. De Leon Gatti M et al (2007) Comparative transcriptional analysis of mouse hybridoma and recombinant Chinese hamster ovary cells undergoing butyrate treatment. J Biosci Bioeng 103(1):82-91
87. Mimura Y et al (2001) Butyrate increases production of human chimeric IgG in CHO-K1 cells whilst maintaining function and glycoform profile. J Immunol Methods 247(1-2): 205-216
88. Korke R et al (2004) Large scale gene expression profiling of metabolic shift of mammalian cells in culture. J Biotechnol 107(1):1-17
89. Lecca MR et al (2005) Genome-wide analysis of the unfolded protein response in fibroblasts from congenital disorders of glycosylation type-I patients. FASEB J 19(2):240-242
90. Wong DC et al (2010) Profiling of N-glycosylation gene expression in CHO cell fed-batch cultures. Biotechnol Bioeng 107(3):516-528
91. Seth G et al (2007) Molecular portrait of high productivity in recombinant NS0 cells. Biotechnol Bioeng 97(4):933-951
92. Shelikoff M, Sinskey AJ, Stephanopoulos G (1994) The effect of protein synthesis inhibitors on the glycosylation site occupancy of recombinant human prolactin. Cytotechnology 15(1-3):195-208
93. Wang WC et al (1991) The poly-N-acetyllactosamines attached to lysosomal membrane glycoproteins are increased by the prolonged association with the Golgi complex. J Biol Chem 266(34):23185-23190
94. Bulleid NJ et al (1992) Cell-free synthesis of enzymically active tissue-type plasminogen activator. Protein folding determines the extent ofN-linked glycosylation. BiochemJ 286(Pt 1): 275-280
95. Grabenhorst E et al (1999) Genetic engineering of recombinant glycoproteins and the glycosylation pathway in mammalian host cells. Glycoconj J 16(2):81-97
96. Comelli EM et al (2006) A focused microarray approach to functional glycomics: transcriptional regulation of the glycome. Glycobiology 16(2):117-131
97. Travers KJ et al (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101(3):249-258
98. Klebl B et al (2001) A comprehensive analysis of gene expression profiles in a yeast N-glycosylation mutant. Biochem Biophys Res Commun 286(4):714-720
99. Cullen PJ et al (2006) Genome-wide analysis of the response to protein glycosylation deficiency in yeast. FEMS Yeast Res 6(8):1264-1273
100. Gerdtzen ZP, Daoutidis P, Hu WS (2004) Non-linear reduction for kinetic models of metabolic reaction networks. Metab Eng 6(2):140-154
101. Umana P, Bailey JE (1997) A mathematical model of N-linked glycoform biosynthesis. Biotechnol Bioeng 55(6):890-908
102. Krambeck FJ, Betenbaugh MJ (2005) A mathematical model of N-linked glycosylation. Biotechnol Bioeng 92(6):711-728
103. Inoue N et al (1999) Asn-linked sugar chain structures of recombinant human thrombopoietin produced in Chinese hamster ovary cells. Glycoconj J 16(11):707-718
104. Hossler P, Mulukutla BC, Hu WS (2007) Systems analysis of N-glycan processing in mammalian cells. PLoS One 2(1):e713
105. Elsner M, Hashimoto H, Nilsson T (2003) Cisternal maturation and vesicle transport: join the band wagon!. Mol Membr Biol 20(3):221-229
106. Marsh BJ, Howell KE (2002) The mammalian Golgi-complex debates. Nat Rev Mol Cell Biol 3(10):789-795
107. Colley KJ (1997) Golgi localization of glycosyltransferases: more questions than answers. Glycobiology 7(1):1-13
108. Hossler P et al (2006) GlycoVis: visualizing glycan distribution in the protein N-glycosylation pathway in mammalian cells. Biotechnol Bioeng 95(5):946-960
109. Spellman MW et al (1989) Carbohydrate structures of human tissue plasminogen activator expressed in Chinese hamster ovary cells. J Biol Chem 264(24):14100-14111
110. Mironov A Jr, Luini A, Mironov A (1998) A synthetic model of intra-Golgi traffic. FASEB J 12(2):249-252
111. Ferrara C et al (2006) Modulation of therapeutic antibody effector functions by glycosylation engineering: influence of Golgi enzyme localization domain and co-expression of heterologous beta1, 4-N-acetylglucosaminyltransferase III and Golgi alpha-mannosidase II. Biotechnol Bioeng 93(5):851-861
112. Monica TJ, Andersen DC, Goochee CF (1997) A mathematical model of sialylation of N-linked oligosaccharides in the trans-Golgi network. Glycobiology 7(4):515-521
113. Shelikoff M, Sinskey AJ, Stephanopoulos G (1996) A modeling framework for the study of protein glycosylation. Biotechnol Bioeng 50(1):73-90
114. Liu G et al (2008) Systems-level modeling of cellular glycosylation reaction networks: O-linked glycan formation on natural selectin ligands. Bioinformatics 24(23):2740-2747
115. Marathe DD et al (2008) Systems-level studies of glycosyltransferase gene expression and enzyme activity that are associated with the selectin binding function of human leukocytes. FASEB J 22(12):4154-4167