Transcriptome analysis of a CHO cell line expressing a recombinant therapeutic protein treated with inducers of protein expression

Journal of Biotechnology

Volumn 212, Issue , 2015, Pages 106-115

  Fomina Yadlin, Dina ^a   Mujacic, Mirna ^a   Maggiora, Kathy ^a   Quesnell, Garrett ^a   Saleem, Ramsey ^a   McGrew, Jeffrey T ^a  

^a AMGEN INC   (United States)

Author keywords

Chinese hamster ovary; Recombinant protein expression; RNA Seq; Small molecule inducers; Specific productivity; Temperature shift

Indexed keywords

BIOLOGICAL SYSTEMS; CELL CULTURE; CELLS; CYTOLOGY; GENE EXPRESSION; GENES; MOLECULES; NUCLEIC ACIDS; PRODUCTIVITY; PROTEINS; RECOMBINANT PROTEINS; RNA; TRANSCRIPTION;

CHINESE HAMSTER OVARY; RECOMBINANT PROTEIN EXPRESSION; SMALL MOLECULES; SPECIFIC PRODUCTIVITY; TEMPERATURE SHIFT;

CELL ENGINEERING;

BUTYRIC ACID; CAFFEINE; DIHYDROFOLATE REDUCTASE; HEXAMETHYLENEBISACETAMIDE; HYBRID PROTEIN; MESSENGER RNA; RANK FC FUSION PROTEIN; RECOMBINANT PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; ACETAMIDE DERIVATIVE; RANK-FC;

ANIMAL CELL; ARTICLE; CELL CYCLE PROGRESSION; CHO CELL LINE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; NEXT GENERATION SEQUENCING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; RNA PROCESSING; RNA SEQUENCE; RNA TRANSLATION; TEMPERATURE SENSITIVITY; TRANSCRIPTOMICS; ANIMAL; CELL SURVIVAL; CRICETULUS; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; HAMSTER; METABOLISM; PROTEOMICS; SEQUENCE ANALYSIS; TEMPERATURE;

ACETAMIDES; ANIMALS; BUTYRIC ACID; CAFFEINE; CELL SURVIVAL; CHO CELLS; CRICETINAE; CRICETULUS; GENE EXPRESSION; GENE EXPRESSION PROFILING; PROTEOMICS; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TEMPERATURE;

EID: 84941092128     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2015.08.025     Document Type: Article

References (57)

1. Allen M.J., Boyce J.P., Trentalange M.T., Treiber D.L., Rasmussen B., Tillotson B., Davis R., Reddy P. Identification of novel small molecule enhancers of protein production by cultured mammalian cells. Biotechnol. Bioeng. 2008, 100:1193-1204.
2. Bavner A., Matthews J., Sanyal S., Gustafsson J.A., Treuter E. EID3 is a novel EID family member and an inhibitor of CBP-dependent co-activation. Nucleic Acids Res. 2005, 33:3561-3569.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B (Methodological) 1995, 289-300.
4. Brosch M., Yu L., Hubbard T., Choudhary J. Accurate and sensitive peptide identification with Mascot Percolator. J. Proteome Res. 2009, 8:3176-3181.
5. Browne S.M., Al-Rubeai M. Selection methods for high-producing mammalian cell lines. Trends Biotechnol. 2007, 25:425-432.
6. Butler M., Meneses-Acosta A. Recent advances in technology supporting biopharmaceutical production from mammalian cells. Appl Microbiol. Biotechnol. 2012, 96:885-894.
7. Clarke C., Doolan P., Barron N., Meleady P., Madden S.F., DiNino D., Leonard M., Clynes M. CGCDB: a web-based resource for the investigation of gene coexpression in CHO cell culture. Biotechnol. Bioeng. 2012, 109:1368-1370.
8. Clrke C., Dooln P., Brron N., Meledy P., O'Sullivn F., Gmmell P., Melville M., Leonrd M., Clynes M. Large scale microrry profiling nd coexpression network nlysis of CHO cells identifies trnscriptionl modules ssocited with growth nd productivity. J. Biotechnol. 2011, 155:350-359.
9. Clarke C., Doolan P., Barron N., Meleady P., O'Sullivan F., Gammell P., Melville M., Leonard M., Clynes M. Predicting cell-specific productivity from CHO gene expression. J. Biotechnol. 2011, 151:159-165.
10. Contreras X., Barboric M., Lenasi T., Peterlin B.M. HMBA releases P-TEFb from HEXIM1 and 7SK snRNA via PI3K/Akt and activates HIV transcription. PLoS Pathog. 2007, 3:1459-1469.
11. Davie J.R. Inhibition of histone deacetylase activity by butyrate. J. Nutr. 2003, 133:2485S-2493S.
12. Davies S.L., Lovelady C.S., Grainger R.K., Racher A.J., Young R.J., James D.C. Functional heterogeneity and heritability in CHO cell populations. Biotechnol. Bioeng. 2013, 110:260-274.
13. De Jesus M., Wurm F.M. Manufacturing recombinant proteins in kg-ton quantities using animal cells in bioreactors. Eur. J. Pharm. Biopharm. Off. J. Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e. V 2011, 78:184-188.
14. Doolan P., Barron N., Kinsella P., Clarke C., Meleady P., O'Sullivan F., Melville M., Leonard M., Clynes M. Microarray expression profiling identifies genes regulating sustained cell specific productivity (S-Qp) in CHO K1 production cell lines. Biotechnol. J. 2012, 7:516-526.
15. Du Z., Treiber D., McCarter J.D., Fomina-Yadlin D., Saleem R.A., McCoy R.E., Zhang Y., Tharmalingam T., Leith M., Follstad B.D., Dell B., Grisim B., Zupke C., Heath C., Morris A.E., Reddy P. Use of a small molecule cell cycle inhibitor to control cell growth and improve specific productivity and product quality of recombinant proteins in CHO cell cultures. Biotechnol. Bioeng. 2014.
16. Eng J.K., McCormack A.L., Yates J.R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 1994, 5:976-989.
17. Fann C.H., Guarna M.M., Kilburn D.G., Piret J.M. Relationship between recombinant activated protein C secretion rates and mRNA levels in baby hamster kidney cells. Biotechnol. Bioeng. 1999, 63:464-472.
18. Fomina-Yadlin D., Du Z., McGrew J.T. Gene expression measurements normalized to cell number reveal large scale differences due to cell size changes, transcriptional amplification and transcriptional repression in CHO cells. J. Biotechnol. 2014.
19. Fox S.R., Patel U.A., Yap M.G., Wang D.I. Maximizing interferon-(production by chinese hamster ovary cells through temperature shift optimization: Experimental and modeling. Biotechnol. Bioeng. 2004, 85:177-184.
20. Fredholm B.B., Battig K., Holmen J., Nehlig A., Zvartau E.E. Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol. Rev. 1999, 51:83-133.
21. Griffin N.M., Yu J., Long F., Oh P., Shore S., Li Y., Koziol J.A., Schnitzer J.E. Label-free, normalized quantification of complex mass spectrometry data for proteomic analysis. Nat. Biotechnol. 2010, 28:83-89.
22. Ho S.C., Bardor M., Li B., Lee J.J., Song Z., Tong Y.W., Goh L.-T., Yang Y. Comparison of Internal Ribosome Entry Site (IRES) and Furin-2A (F2A) for monoclonal antibody expression level and quality in CHO cells. PLoS One 2013, 8:e63247.
23. Jeon M.K., Lee G.M. Correlation between enhancing effect of sodium butyrate on specific productivity and mRNA transcription level in recombinant Chinese hamster ovary cells producing antibody. J. Microbiol. Biotechnol. 2007, 17:1036-1040.
24. Jiang Z., Huang Y., Sharfstein S.T. Regulation of recombinant monoclonal antibody production in chinese hamster ovary cells: a comparative study of gene copy number, mRNA level, and protein expression. Biotechnol. Prog. 2006, 22:313-318.
25. Kang S., Ren D., Xiao G., Daris K., Buck L., Enyenihi A.A., Zubarev R., Bondarenko P.V., Deshpande R. Cell line profiling to improve monoclonal antibody production. Biotechnol. Bioeng. 2014, 111:748-760.
26. Kantardjieff A., Jacob N.M., Yee J.C., Epstein E., Kok Y.J., Philp R., Betenbaugh M., Hu W.S. Transcriptome and proteome analysis of Chinese hamster ovary cells under low temperature and butyrate treatment. J. Biotechnol. 2010, 145:143-159.
27. Kim Y.B., Lee K.H., Sugita K., Yoshida M., Horinouchi S. Oxamflatin is a novel antitumor compound that inhibits mammalian histone deacetylase. Oncogene 1999, 18:2461-2470.
28. Lee C.J., Seth G., Tsukuda J., Hamilton R.W. A clone screening method using mRNA levels to determine specific productivity and product quality for monoclonal antibodies. Biotechnol. Bioeng. 2009, 102:1107-1118.
29. Lewis N.E., Liu X., Li Y., Nagarajan H., Yerganian G., O'Brien E., Bordbar A., Roth A.M., Rosenbloom J., Bian C., Xie M., Chen W., Li N., Baycin-Hizal D., Latif H., Forster J., Betenbaugh M.J., Famili I., Xu X., Wang J., Palsson B.O. Genomic landscapes of Chinese hamster ovary cell lines as revealed by the Cricetulus griseus draft genome. Nat. Biotechnol. 2013, 31:759-765.
30. Loven J., Orlando D.A., Sigova A.A., Lin C.Y., Rahl P.B., Burge C.B., Levens D.L., Lee T.I., Young R.A. Revisiting global gene expression analysis. Cell 2012, 151:476-482.
31. McGrew J.T. Vectors and Methods for Recombinant Protein Expression 2003, Immunex Corporation, US.
32. McLeod J., O'Callaghan P.M., Pybus L.P., Wilkinson S.J., Root T., Racher A.J., James D.C. An empirical modeling platform to evaluate the relative control discrete CHO cell synthetic processes exert over recombinant monoclonal antibody production process titer. Biotechnol. Bioeng. 2011, 108:2193-2204.
33. Mimura Y., Lund J., Church S., Dong S., Li J., Goodall M., Jefferis R. Butyrate increases production of human chimeric IgG in CHO-K1 cells whilst maintaining function and glycoform profile. J. Immunol. Methods 2001, 247:205-216.
34. Mortazavi A., Williams B.A., McCue K., Schaeffer L., Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 2008, 5:621-628.
35. Nam J.H., Zhang F., Ermonval M., Linhardt R.J., Sharfstein S.T. The effects of culture conditions on the glycosylation of secreted human placental alkaline phosphatase produced in Chinese hamster ovary cells. Biotechnol. Bioeng. 2008, 100:1178-1192.
36. Nissom P.M., Sanny A., Kok Y.J., Hiang Y.T., Chuah S.H., Shing T.K., Lee Y.Y., Wong K.T., Hu W.S., Sim M.Y., Philp R. Transcriptome and proteome profiling to understanding the biology of high productivity CHO cells. Mol. Biotechnol. 2006, 34:125-140.
37. Oleinick N.L. The initiation and elongation steps in protein synthesis: relative rates in Chinese hamster ovary cells during and after hyperthermic and hypothermic shocks. J. Cell. Physiol. 1979, 98:185-192.
38. Paterson T., Innes J., Moore S. Approaches to maximizing stable expression of alpha 1-antitrypsin in transformed CHO cells. Appl. Microbiol. Biotechnol. 1994, 40:691-698.
39. Porter A.J., Racher A.J., Preziosi R., Dickson A.J. Strategies for selecting recombinant CHO cell lines for cGMP manufacturing: improving the efficiency of cell line generation. Biotechnol. Prog. 2010, 26:1455-1464.
40. Risso D., Ngai J., Speed T.P., Dudoit S. Normalization of RNA- seq data using factor analysis of control genes or samples. Nat. Biotech. Adv. Online Publ. 2014.
41. Schlatter S., Stansfield S.H., Dinnis D.M., Racher A.J., Birch J.R., James D.C. On the optimal ratio of heavy to light chain genes for efficient recombinant antibody production by CHO cells. Biotechnol. Prog. 2005, 21:122-133.
42. Seth G., Charaniya S., Wlaschin K.F., Hu W.S. In pursuit of a super producer-alternative paths to high producing recombinant mammalian cells. Curr. Opin. Biotechnol. 2007, 18:557-564.
43. Seth G., Philp R.J., Lau A., Jiun K.Y., Yap M., Hu W.S. Molecular portrait of high productivity in recominant NS0 cells. Biotechnol. Bioeng. 2007, 97:933-951.
44. Sordillo E.M., Pearse R.N. RANK-Fc: a therapeutic antagonist for RANK-L in myeloma. Cancer 2003, 97:802-812.
45. Sou S.N., Sellick C., Lee K., Mason A., Kyriakopoulos S., Polizzi K.M., Kontoravdi C. How does mild hypothermia affect monoclonal antibody glycosylation?. Biotechnol. Bioeng. 2014.
46. Stamminger T., Fickenscher H., Fleckenstein B. Cell type-specific induction of the major immediate early enhancer of human cytomegalovirus by cyclic AMP. J. Gen. Virol. 1990, 71:105-113. Pt 1).
47. Sunley K., Butler M. Strategies for the enhancement of recombinant protein production from mammalian cells by growth arrest. Biotechnol. Adv. 2010, 28:385-394.
48. Takahashi K., Satani M., Harada S., Noguchi M. Expression and characterization of frog peptidylglycine alpha- hydroxylating monooxygenase. Protein Expr. Purif. 2003, 27:35-41.
49. Van Ness K.P., Trentalange M.T., Dell B.D., McGrew J.T. Methods for Increasing Polypeptide Production 2008, US, Immunex Corporation.
50. Vishwnthn N., Le H., Jcob N.M., Tso Y.S., Ng S.W., Loo B., Liu Z., Kntrdjieff A., Hu W.S. Trnscriptome dynmics of trnsgene mplifiction in Chinese hmster ovry cells. Biotechnology nd bioengineering 2014, 111:518-528.
51. Vishwanathan N., Le H., Le T., Hu W.S. Advancing iopharmaceutical process science through transcriptome analysis. Curr. Opin. Biotechnol. 2014, 30C:113-119.
52. Vlach J., Pitha P.M. Hexamethylene bisacetamide activates the human immunodeficiency virus type 1 provirus by an NF-kappa B-independent mechanism. J. Gen. Virol. 1993, 74(Pt 11):2401-2408.
53. Wulhfard S., Baldi L., Hacker D.L., Wurm F. Valproic acid enhances recombinant mRNA and protein levels in transiently transfected Chinese hamster ovary cells. J. Biotechnol. 2010, 148:128-132.
54. Wulhfard S., Tissot S., Bouchet S., Cevey J., De Jesus M., Hacker D.L., Wurm F.M. Mild hypothermia improves transient gene expression yields several fold in Chinese hamster ovary cells. Biotechnol. Prog. 2008, 24:458-465.
55. Yang W.C., Lu J., Nguyen N.B., Zhang A., Healy N.V., Kshirsagar R., Ryll T., Huang Y.M. Addition of valproic acid to CHO cell fed-batch cultures improves monoclonal antibody titers. Mol. Biotechnol. 2014, 56:421-428.
56. Yee J.C., de Leon Gatti M., Philp R.J., Yap M., Hu W.S. Genomic and proteomic exploration of CHO and hybridoma cells under sodium butyrate treatment. Biotechnol. Bioeng. 2008, 99:1186-1204.
57. Yee J.C., Gerdtzen Z.P., Hu W.S. Comparative transcriptome analysis to unveil genes affecting recombinant protein productivity in mammalian cells. Biotechnol. Bioeng. 2009, 102:246-263.