Understanding of altered N-glycosylation-related gene expression in recombinant Chinese hamster ovary cells subjected to elevated ammonium concentration by digital mRNA counting

Biotechnology and Bioengineering

Volumn 112, Issue 8, 2015, Pages 1583-1593

  Ha, Tae Kwang ^a   Kim, Yeon Gu ^b   Lee, Gyun Min ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Ammonium; CHO cells; Fc fusion protein; N glycosylation; Nanostring nCounter system

Indexed keywords

CARBOXYLIC ACIDS; CELLS; CYTOLOGY; ELECTROPHORESIS; ESTERIFICATION; GENES; GLYCOSYLATION; PROTEINS; RECOMBINANT PROTEINS;

AMMONIUM; CHO CELL; FC FUSION PROTEINS; N-GLYCOSYLATION; NANOSTRING NCOUNTER SYSTEM;

GENE EXPRESSION;

AMMONIA; GLUTAMINE; HYBRID PROTEIN; MESSENGER RNA; SIALIC ACID; SIALIDASE; SIALIDASE 1; SIALIDASE 3; UNCLASSIFIED DRUG; AMMONIUM DERIVATIVE; CULTURE MEDIUM; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL VIABILITY; CHINESE HAMSTER; CHO CELL LINE; CONTROLLED STUDY; DIGITAL IMAGING; DOWN REGULATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE SILENCING; NONHUMAN; OVARY CELL; PH; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; RNA ANALYSIS; SIALYLATION; TRANSIENT EXPRESSION; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL PROLIFERATION; CHEMISTRY; CRICETULUS; CULTURE MEDIUM; CULTURE TECHNIQUE; FEMALE; GENETICS; GLYCOSYLATION; METABOLISM; PROCEDURES;

CRICETULUS GRISEUS;

AMMONIUM COMPOUNDS; ANIMALS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CHO CELLS; CRICETULUS; CULTURE MEDIA; FEMALE; GENE EXPRESSION; GLYCOSYLATION; RECOMBINANT PROTEINS; RNA, MESSENGER;

EID: 84932199513     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25568     Document Type: Article

References (37)

1. 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.
2. 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.
3. Borys MC, Linzer DI, Papoutsakis ET. 1993. Culture pH affects expression rates and glycosylation of recombinant mouse placental lactogen proteins by Chinese hamster ovary (CHO) cells. Biotechnology 11(6):720-724.
4. Chen P, Harcum SW. 2006. Effects of elevated ammonium on glycosylation gene expression in CHO cells. Metab Eng 8(2):123-132.
5. Del Prete MJ, Robles MS, Guáo A, Martínez-A C, Izquierdo M, Garcia-Sanz JA. 2002. Degradation of cellular mRNA is a general early apoptosis-induced event. FASEB J 16(14):2003-2005.
6. Elliott S, Lorenzini T, Asher S, Aoki K, Brankow D, Buck L, Busse L, Chang D, Fuller J, Grant J, Hernday N, Hokum M, Hu S, Knudten A, Levin N, Komorowski R, Martin F, Navarro R, Osslund T, Rogers G, Rogers N, Trail G, Egrie J. 2003. Enhancement of therapeutic protein in vivo activities through glycoengineering. Nat Biotechnol 21(14):414-421.
7. Gawlitzek M, Ryll T, Lofgren J, Sliwkowski MB. 2000. Ammonium alters N-glycan structures of recombinant TNFR-IgG: degradative versus biosynthetic mechanisms. Biotechnol Bioeng 68(6):637-646.
8. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, Fell HP, Ferree S, George RD, Grogan T, James JJ, Maysuria M, Mitton JD, Oliveri P, Osborn JL, Peng T, Ratcliffe AL, Webster PJ, Davidson EH, Hood L, Dimitrov K. 2008. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 26(3):317-325.
9. Gramer MJ, Goochee CF. 1993. Glycosidase activities in Chinese hamster ovary cell lysate and cell culture supernatant. Biotechnol Prog 9(4):366-373.
10. Ha TK, Lee GM. 2014. Effect of glutamine substitution by TCA cycle intermediates on the production and sialylation of Fc-fusion protein in Chinese hamster ovary cell culture. J Biotechnol 180:23-29.
11. Hong JK, Cho SM, Yoon SK. 2010. Substitution of glutamine by glutamate enhances production and galactosylation of recombinant IgG in Chinese hamster ovary cells. Appl Microbiol Biotechnol 88(4):869-879.
12. Hossler P, Khattak SF, Li ZJ. 2009. Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology 19(19):936-949.
13. Hwang SO, Lee GM. 2008. Nutrient deprivation induces autophagy as well as apoptosis in Chinese hamster ovary cell culture. Biotechnol Bioeng 99(3):678-685.
14. Jenkins N, Parekh RB, James DC. 1996. Getting the glycosylation right: Implications for the biotechnology industry. Nat Biotechnol 14(8):975-981.
15. Jeong YT, Choi O, Son YD, Park SY, Kim JH. 2009. Enhanced sialylation of recombinant erythropoietin in genetically engineered Chinese-hamster ovary cells. Biotechnol Appl Biochem 52(Pt 4):283-291.
16. Lawrence SM, Huddleston KA, Pitts LR, Nguyen N, Lee YC, Vann WF, Coleman TA, Betenbaugh MJ. 2000. Cloning and expression of the human N-acetylneuraminic acid phosphate synthase gene with 2-keto-3-deoxy-D-glycero- D-galacto-nononic acid biosynthetic ability. J Biol Chem 275(23):17869-17877.
17. Lee J, Sundaram S, Shaper NL, Raju TS, Stanley P. 2001. Chinese hamster ovary (CHO) cells may express six beta 4-galactosyltransferases (beta 4GalTs). Consequences of the loss of functional beta 4GalT-1, beta 4GalT-6, or both in CHO glycosylation mutants. J Biol Chem 276(17):13924-13934.
18. Lee SM, Kim YG, Lee EG, Lee GM. 2014. Digital mRNA profiling of N-glycosylation gene expression in recombinant Chinese hamster ovary cells treated with sodium butyrate. J Biotechnol 171:56-60.
19. Lewis NE, Liu X, Li Y, Nagarajan H, Yerganian G, O'Brien E, Bordbar A, Roth AM, Rosenbloom J, Bian C, Xie M, Chen W, Li N, Baycin-Hizal D, Latif H, Forster J, Betenbaugh MJ, Famili I, Xu X, Wang J, Palsson BO. 2013. Genomic landscapes of Chinese hamster ovary cell lines as revealed by the Cricetulus griseus draft genome. Nat Biotechnol 31(8):759-765.
20. Lipscomb ML, Palomares LA, Hernández V, Ramírez OT, Kompala DS. 2005. Effect of production method and gene amplification on the glycosylation pattern of a secreted reporter protein in CHO cells. Biotechnol Prog 21(1):40-49.
21. Narimatsu H, Sinha S, Brew K, Okayama H, Qasba PK. 1986. Cloning and sequencing of cDNA of bovine N-acetylglucosamine (beta 1-4) galactosyltransferase. Proc Natl Acad Sci USA 83(13):4720-4724.
22. Noh SM, Sathyamurthy M, Lee GM. 2013. Development of recombinant Chinese hamster ovary cell lines for therapeutic protein production. Curr Opin Chem Eng 2(5):391-397.
23. Renard JM, Spagnoli R, Mazier C, Salles MF, Mandine E. 1988. Evidence that monoclonal antibody production kinetics is related to the integral of the viable cells curve in batch systems. Biotechnol Lett 10(2):91-96.
24. Restelli V, Wang MD, Huzel N, Ethier M, Perreault H, Butler M. 2006. The effect of dissolved oxygen on the production and the glycosylation profile of recombinant human erythropoietin produced from CHO cells. Biotechnol Bioeng 94(3):481-494.
25. Schneider M, Marison IW, von Stockar U. 1996. The importance of ammonia in mammalian cell culture. J Biotechnol 46(3):161-185.
26. Shaper NL, Shaper JH, Meuth JL, Fox JL, Chang H, Kirsch IR, Hollis GF. 1986. Bovine galactosyltransferase: Identification of a clone by direct immunological screening of a cDNA expression library. Proc Natl Acad Sci USA 83(6):1573-1577.
27. Sung YH, Song YJ, Lim SW, Chung JY, Lee GM. 2004. Effect of sodium butyrate on the production, heterogeneity and biological activity of human thrombopoietin by recombinant Chinese hamster ovary cells. J Biotechnol 112(3):323-335.
28. Suzuki S, Matsuzawa T, Nukigi Y, Takegawa K, Tanaka N. 2010. Characterization of two different types of UDP-glucose/-galactose 4-epimerase involved in galactosylation in fission yeast. Microbiology 156(Pt 3):708-718.
29. 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.
30. Valley U, Nimtz M, Conradt HS, Wagner R. 1999. Incorporation of ammonium into intracellular UDP-activated N-acetylhexosamines and into carbohydrate structures in glycoproteins. Biotechnol Bioeng 64(4):401-417.
31. Wong NS, Wati L, Nissom PM, Feng HT, Lee MM, Yap MG. 2010. An investigation of intracellular glycosylation activities in CHO cells: Effects of nucleotide sugar precursor feeding. Biotechnol Bioeng 107(2):321-336.
32. Yang M, Butler M. 2000. Effects of ammonia on CHO cell growth, erythropoietin production, and glycosylation. Biotechnol Bioeng 68(4):370-380.
33. Yang M, Butler M. 2002. Effects of ammonia and glucosamine on the heterogeneity of erythropoietin glycoforms. Biotechnol Prog 18(1):129-138.
34. 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.
35. Xu X, Nagarajan H, Lewis NE, Pan S, Cai Z, Liu X, Chen W, Xie M, Wang W, Hammond S, Andersen MR, Neff N, Passarelli B, Koh W, Fan HC, Wang J, Gui Y, Lee KH, Betenbaugh MJ, Quake SR, Famili I, Palsson BO, Wang J. 2011. The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line. Nat Biotechnol 29(8):735-741.
36. Zhang P, Tan DL, Heng D, Wang T, Mariati, Yang Y, Song Z. 2010. A functional analysis of N-glycosylation-related genes on sialylation of recombinant erythropoietin in six commonly used mammalian cell lines. Metab Eng 12(6):526-536.
37. Zhang M, Koskie K, Ross JS, Kayser KJ, Caple MV. 2010b. Enhancing glycoprotein sialylation by targeted gene silencing in mammalian cells. Biotechnol Bioeng 105(6):1094-1105.