Global phosphoproteomic study of high/low specific productivity industrially relevant mAb producing recombinant CHO cell lines

Abelin, 2016, Reduced-representation phosphosignatures measured by quantitative targeted MS capture cellular states and enable large-scale comparison of drug-induced phenotypes, Mol. Cell. Proteomics, 15, 1622, 10.1074/mcp.M116.058354 Angel, 2012, Mass spectrometry-based proteomics: existing capabilities and future directions, Chem. Soc. Rev., 41, 3912, 10.1039/c2cs15331a Blethrow, 2008, Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates, Proc. Natl. Acad. Sci. USA, 105, 1442, 10.1073/pnas.0708966105 Brinkrolf, 2013, Chinese hamster genome sequenced from sorted chromosomes, Nat. Biotechnol., 31, 694, 10.1038/nbt.2645 Brunn, 1997, Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin, Science (80-.), 277, 99, 10.1126/science.277.5322.99 Case, 2011, Mechanical regulation of glycogen synthase kinase 3beta (GSK3beta) in mesenchymal stem cells is dependent on Akt protein serine 473 phosphorylation via mTORC2 protein, J. Biol. Chem., 286, 39450, 10.1074/jbc.M111.265330 Castilho, 2014, Keeping the eIF2 alpha kinase Gcn2 in check, BBA, 1843, 1948 Choudhary, 2010, Decoding signalling networks by mass spectrometry-based proteomics, Nat. Rev. Mol. Cell Biol., 11, 427, 10.1038/nrm2900 Clarke, 2011, Predicting cell-specific productivity from CHO gene expression, J. Biotechnol., 151, 159, 10.1016/j.jbiotec.2010.11.016 Cohen, 2000, The regulation of protein function by multisite phosphorylation–a 25 year update, Trends Biochem. Sci., 25, 596, 10.1016/S0968-0004(00)01712-6 Coleman, O., Henry, M., Clynes, M., Meleady, P., 2017. Filter-Aided Sample Preparation (FASP) for Improved Proteome Analysis of Recombinant Chinese Hamster Ovary Cells BT - Heterologous Protein Production in CHO Cells: Methods and Protocols. In: Meleady, P. (Ed.), Springer New York, New York, NY, pp. 187–194. Datta, 2013, An ’omics approach towards CHO cell engineering, Biotechnol. Bioeng., 110, 1255, 10.1002/bit.24841 Dobrikov, 2011, Phosphorylation of eukaryotic translation initiation factor 4G1 (eIF4G1) by protein kinase Cα regulates eIF4G1 binding to Mnk1, Mol. Cell. Biol., 31, 2947, 10.1128/MCB.05589-11 Dobrikov, 2014, Mitotic phosphorylation of eukaryotic initiation factor 4G1 (eIF4G1) at Ser1232 by Cdk1:cyclin B inhibits eIF4A helicase complex binding with RNA, Mol. Cell. Biol., 34, 439, 10.1128/MCB.01046-13 Dreesen, 2011, Ectopic expression of human mTOR increases viability, robustness, cell size, proliferation, and antibody production of chinese hamster ovary cells, Biotechnology and bioengineering, 108, 853, 10.1002/bit.22990 Du, 2015, 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, Biotechnology and bioengineering, 112, 141, 10.1002/bit.25332 Garcia-Barrio, 2002, Serine 577 is phosphorylated and negatively affects the tRNA binding and eIF2alpha kinase activities of GCN2, J. Biol. Chem., 277, 30675, 10.1074/jbc.M203187200 Grav, 2018, Minimizing clonal variation during mammalian cell line engineering for improved systems biology data generation, ACS Synth. Biol., 7, 2148, 10.1021/acssynbio.8b00140 Gutierrez, 2015, Optimizing eukaryotic cell hosts for protein production through systems biotechnology and genome-scale modeling, Biotechnol. J., 10, 939, 10.1002/biot.201400647 Henry, 2017, Differential phosphoproteomic analysis of recombinant Chinese hamster ovary cells following temperature shift, J. Proteome Res., 16, 2339, 10.1021/acs.jproteome.6b00868 Imami, 2018, Phosphorylation of the Ribosomal Protein RPL12/uL11 Affects Translation during Mitosis, Mol. Cell, 72, 84, 10.1016/j.molcel.2018.08.019 Kaas, 2015, Sequencing the CHO DXB11 genome reveals regional variations in genomic stability and haploidy, BMC Genomics, 16, 160, 10.1186/s12864-015-1391-x Kaushik, 2018, The expression pattern of the phosphoproteome is significantly changed during the growth phases of recombinant CHO cell culture, Biotechnol. J., 13, e1700221, 10.1002/biot.201700221 Kelly, 2018, Modulation of IgG1 immunoeffector function by glycoengineering of the GDP-fucose biosynthesis pathway, Biotechnol. Bioeng., 115, 705, 10.1002/bit.26496 Kim, 2017, Control of leucine-dependent mTORC1 pathway through chemical intervention of leucyl-tRNA synthetase and RagD interaction, Nat. Commun., 8, 732, 10.1038/s41467-017-00785-0 Kim, 2012, CHO cells in biotechnology for production of recombinant proteins: Current state and further potential, Appl. Microbiol. Biotechnol., 93, 917, 10.1007/s00253-011-3758-5 Lee, 2015, CRISPR/Cas9-mediated genome engineering of CHO cell factories: Application and perspectives, Biotechnology Journal, 10, 979, 10.1002/biot.201500082 Lewis, 2013, Genomic landscapes of Chinese hamster ovary cell lines as revealed by the Cricetulus griseus draft genome, Nat. Biotechnol., 31, 759, 10.1038/nbt.2624 Li, 2013, Elucidating human phosphatase-substrate networks, Sci. Signal., 6, rs10, 10.1126/scisignal.2003203 Lu, 2014, Loss of the eukaryotic initiation factor 2α kinase general control nonderepressible 2 protects mice from pressure overload-induced congestive heart failure without affecting ventricular hypertrophy, Hypertens (Dallas, Tex. 1979), 63, 128, 10.1161/HYPERTENSIONAHA.113.02313 Marintchev, 2005, eIF4G and CBP80 share a common origin and similar domain organization: implications for the structure and function of eIF4G, Biochemistry, 44, 12265, 10.1021/bi051271v Nissom, 2006, Transcriptome and proteome profiling to understanding the biology of high productivity CHO cells, Mol. Biotechnol., 34, 125, 10.1385/MB:34:2:125 Shahbazian, 2010, eIF4B controls survival and proliferation and is regulated by proto-oncogenic signaling pathways, Cell Cycle, 9, 4106, 10.4161/cc.9.20.13630 Smales, 2004, Comparative proteomic analysis of GS-NS0 murine myeloma cell lines with varying recombinant monoclonal antibody production rate, Biotechnol. Bioeng., 88, 474, 10.1002/bit.20272 Taus, 2011, Universal and confident phosphorylation site localization using phosphoRS, J. Proteome Res., 10, 5354, 10.1021/pr200611n Visweswaraiah, 2011, Evidence that eukaryotic translation elongation factor 1A (eEF1A) binds the Gcn2 protein C terminus and inhibits Gcn2 activity, J. Biol. Chem., 286, 36568, 10.1074/jbc.M111.248898 Vyse, 2017, Advances in mass spectrometry based strategies to study receptor tyrosine kinases, IUCrJ, 4, 119, 10.1107/S2052252516020546 Walsh, 2014, Biopharmaceutical benchmarks 2014, Nat. Biotechnol., 32, 992, 10.1038/nbt.3040 Walsh, 2018, Biopharmaceutical benchmarks 2018, Nat. Biotechnol., 36, 1136, 10.1038/nbt.4305 Wurm, 2004, Production of recombinant protein therapeutics in cultivated mammalian cells, Nat. Biotechnol., 22, 1393, 10.1038/nbt1026 Xu, 2011, The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line, Nat. Biotechnol., 29, 735, 10.1038/nbt.1932