Absolute quantification of viral proteins during single-round replication of MDCK suspension cells

2008, Update: influenza activity--United States, September 28–November 29, 2008, MMWR Morb. Mortal. Wkly Rep., 57, 1329 Aunins, 2018, Intracellular hepatitis C virus modeling predicts infection dynamics and viral protein mechanisms, J. Virol., 92, 10.1128/JVI.02098-17 Baas, 2006, Integrated molecular signature of disease: analysis of influenza virus-infected macaques through functional genomics and proteomics, J. Virol., 80, 10813, 10.1128/JVI.00851-06 Bissinger, 2019, Semi-perfusion cultures of suspension MDCK cells enable high cell concentrations and efficient influenza A virus production, Vaccine, 37, 7003, 10.1016/j.vaccine.2019.04.054 Bragstad, 2019, Community spread and late season increased incidence of oseltamivir-resistant influenza A(H1N1) viruses in Norway 2016, Influenza Other Respir. Viruses, 13, 372, 10.1111/irv.12637 Brownridge, 2011, The importance of the digest: proteolysis and absolute quantification in proteomics, Methods, 54, 351, 10.1016/j.ymeth.2011.05.005 Buckland, 2014, Technology transfer and scale-up of the Flublok recombinant hemagglutinin (HA) influenza vaccine manufacturing process, Vaccine, 32, 5496, 10.1016/j.vaccine.2014.07.074 Cheung, 2007, Biology of influenza a virus, Ann. N. Y. Acad. Sci., 1102, 1, 10.1196/annals.1408.001 Choppin, 1975, Reproduction of paramyxoviruses, 95 Coombs, 2010, Quantitative proteomic analyses of influenza virus-infected cultured human lung cells, J. Virol., 84, 10888, 10.1128/JVI.00431-10 DeVincenzo, 2010, Viral load drives disease in humans experimentally infected with respiratory syncytial virus, Am. J. Respir. Crit. Care Med., 182, 1305, 10.1164/rccm.201002-0221OC Donis, 2014, Performance characteristics of qualified cell lines for isolation and propagation of influenza viruses for vaccine manufacturing, Vaccine, 32, 6583, 10.1016/j.vaccine.2014.06.045 Douglas, 1976, Influenza: the disease and its complications, Hosp. Pract., 11, 43, 10.1080/21548331.1976.11707045 Dove, 2012, A quantitative proteomic analysis of lung epithelial (A549) cells infected with 2009 pandemic influenza A virus using stable isotope labelling with amino acids in cell culture, Proteomics, 12, 1431, 10.1002/pmic.201100470 Eyers, 2011, CONSeQuence: prediction of reference peptides for absolute quantitative proteomics using consensus machine learning approaches, Mol. Cell. Proteomics, 10, 10.1074/mcp.M110.003384 Fields, 2001 1975 Frensing, 2016, Influenza virus intracellular replication dynamics, release kinetics, and particle morphology during propagation in MDCK cells, Appl. Microbiol. Biotechnol., 100, 7181, 10.1007/s00253-016-7542-4 Gallo-Ramírez, 2015, Bioreactor concepts for cell culture-based viral vaccine production, Expert. Rev. Vaccines, 14, 1181, 10.1586/14760584.2015.1067144 Getie-Kebtie, 2013, Label-free mass spectrometry-based quantification of hemagglutinin and neuraminidase in influenza virus preparations and vaccines, Influenza Other Respir. Viruses, 7, 521, 10.1111/irv.12001 Gillet, 2012, Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis, Mol. Cell. Proteomics, 11, 10.1074/mcp.O111.016717 Heldt, 2015, Single-cell analysis and stochastic modelling unveil large cell-to-cell variability in influenza A virus infection, Nat. Commun., 6, 8938, 10.1038/ncomms9938 Hilleman, 2000, Vaccines in historic evolution and perspective: a narrative of vaccine discoveries, Vaccine, 18, 1436, 10.1016/S0264-410X(99)00434-X Honda, 1988, RNA polymerase of influenza virus: role of NP in RNA chain elongation, J. Biochem., 104, 1021, 10.1093/oxfordjournals.jbchem.a122569 Huang, 2015, Serum-free suspension culture of MDCK cells for production of influenza H1N1 vaccines, PLoS One, 10 Hurt, 2009, Zanamivir-resistant influenza viruses with a novel neuraminidase mutation, J. Virol., 83, 10366, 10.1128/JVI.01200-09 Hutchinson, 2014, Conserved and host-specific features of influenza virion architecture, Nat. Commun., 5, 4816, 10.1038/ncomms5816 Hutchinson, 2010, Genome packaging in influenza a virus, J. Gen. Virol., 91, 313, 10.1099/vir.0.017608-0 Ippoushi, 2016, Absolute quantification of Pru av 2 in sweet cherry fruit by liquid chromatography/tandem mass spectrometry with the use of a stable isotope-labelled peptide, Food Chem., 204, 129, 10.1016/j.foodchem.2016.02.115 Iuliano, 2018, Estimates of global seasonal influenza-associated respiratory mortality: a modelling study, Lancet, 391, 1285, 10.1016/S0140-6736(17)33293-2 Jung, 2010, Reverse genetic platform for inactivated and live-attenuated influenza vaccine, Exp. Mol. Med., 42, 116, 10.3858/emm.2010.42.2.013 Kalbfuss, 2008, Monitoring influenza virus content in vaccine production: precise assays for the quantitation of hemagglutination and neuraminidase activity, Biologicals, 36, 145, 10.1016/j.biologicals.2007.10.002 Kawakami, 2011, Strand-specific real-time RT-PCR for distinguishing influenza vRNA, cRNA, and mRNA, J. Virol. Methods, 173, 1, 10.1016/j.jviromet.2010.12.014 Kettenbach, 2011, Absolute quantification of protein and post-translational modification abundance with stable isotope-labeled synthetic peptides, Nat. Protoc., 6, 175, 10.1038/nprot.2010.196 Kummer, 2014, Alteration of protein levels during influenza virus H1N1 infection in host cells: a proteomic survey of host and virus reveals differential dynamics, PLoS One, 9, 10.1371/journal.pone.0094257 Kupke, 2019, A novel type of influenza a virus-derived defective interfering particle with nucleotide substitutions in its genome, J. Virol., 93, 10.1128/JVI.01786-18 Kyaw Win, 2020, Epidemic of influenza A(H1N1)pdm09 analyzed by full genome sequences and the first case of oseltamivir-resistant strain in Myanmar 2017, PLoS One, 15, 10.1371/journal.pone.0229601 Lamb, 2019, Cell-based Quadrivalent inactivated influenza virus vaccine (Flucelvax® tetra/Flucelvax Quadrivalent®): a review in the prevention of influenza, Drugs, 79, 1337, 10.1007/s40265-019-01176-z Lange, 2008, Selected reaction monitoring for quantitative proteomics: a tutorial, Mol. Syst. Biol., 4, 222, 10.1038/msb.2008.61 Laske, 2019, Model-based analysis of influenza A virus replication in genetically engineered cell lines elucidates the impact of host cell factors on key kinetic parameters of virus growth, PLoS Comput. Biol., 15, 10.1371/journal.pcbi.1006944 Liu, 2012, Proteome alterations in primary human alveolar macrophages in response to influenza a virus infection, J. Proteome Res., 11, 4091, 10.1021/pr3001332 Lohr, 2012, Live attenuated influenza viruses produced in a suspension process with avian AGE1.CR.pIX cells, BMC Biotechnol., 12, 79, 10.1186/1472-6750-12-79 Maaß, 2016, Methods and applications of absolute protein quantification in microbial systems, J. Proteome, 136, 222, 10.1016/j.jprot.2016.01.015 MacLean, 2010, Skyline: an open source document editor for creating and analyzing targeted proteomics experiments, Bioinformatics, 26, 966, 10.1093/bioinformatics/btq054 Martin, 1991, Transport of incoming influenza virus nucleocapsids into the nucleus, J. Virol., 65, 232, 10.1128/jvi.65.1.232-244.1991 Matsuda, 2020, Production of influenza virus-like particles using recombinant insect cells, Biochem. Eng. J., 163, 10.1016/j.bej.2020.107757 Matsuoka, 2013, A comprehensive map of the influenza A virus replication cycle, BMC Syst. Biol., 7, 97, 10.1186/1752-0509-7-97 Nicolson, 2005, Generation of influenza vaccine viruses on Vero cells by reverse genetics: an H5N1 candidate vaccine strain produced under a quality system, Vaccine, 23, 2943, 10.1016/j.vaccine.2004.08.054 Nilsson-Payant, 2021, Reduced nucleoprotein availability impairs negative-sense RNA virus replication and promotes host recognition, J. Virol., 95, 10.1128/JVI.02274-20 Norrgran, 2009, Optimization of digestion parameters for protein quantification, Anal. Biochem., 393, 48, 10.1016/j.ab.2009.05.050 Petiot, 2011, Metabolic and kinetic analyses of influenza production in perfusion HEK293 cell culture, BMC Biotechnol., 11, 84, 10.1186/1472-6750-11-84 Popov, 1975, Eine störungsfreie Mikromethode zur Bestimmung des Proteingehaltes in Gewebehomogenaten, Acta Biol. Med. Ger., 34, 1441 Portela, 2002, The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication, J. Gen. Virol., 83, 723, 10.1099/0022-1317-83-4-723 Pralow, 2021, Comprehensive N-glycosylation analysis of the influenza a virus proteins HA and NA from adherent and suspension MDCK cells, FEBS J., 10.1111/febs.15787 Rabe, 2011, Understanding protein adsorption phenomena at solid surfaces, Adv. Colloid Interf. Sci., 162, 87, 10.1016/j.cis.2010.12.007 Richter, 2021, Adsorption of bacteriophages on polypropylene labware affects the reproducibility of phage research, Sci. Rep., 11, 7387, 10.1038/s41598-021-86571-x Ritter, 2010, Metabolic effects of influenza virus infection in cultured animal cells: intra- and extracellular metabolite profiling, BMC Syst. Biol., 4, 61, 10.1186/1752-0509-4-61 Rödig, 2013, Impact of cultivation conditions on N-glycosylation of influenza virus a hemagglutinin produced in MDCK cell culture, Biotechnol. Bioeng., 110, 1691, 10.1002/bit.24834 Roedig, 2011, Impact of host cell line adaptation on quasispecies composition and glycosylation of influenza a virus hemagglutinin, PLoS One, 6, 10.1371/journal.pone.0027989 Rüdiger, 2019, Multiscale modeling of influenza a virus replication in cell cultures predicts infection dynamics for highly different infection conditions, PLoS Comput. Biol., 15, 10.1371/journal.pcbi.1006819 Schulze-Horsel, 2008, Flow cytometric monitoring of influenza a virus infection in MDCK cells during vaccine production, BMC Biotechnol., 8, 45, 10.1186/1472-6750-8-45 Schwahn, 2010, Typing of human and animal strains of influenza virus with conserved signature peptides of matrix M1 protein by high resolution mass spectrometry, J. Virol. Methods, 165, 178, 10.1016/j.jviromet.2010.01.015 Schwarzer, 2009, Glycan analysis in cell culture-based influenza vaccine production: influence of host cell line and virus strain on the glycosylation pattern of viral hemagglutinin, Vaccine, 27, 4325, 10.1016/j.vaccine.2009.04.076 Shapiro, 1987, Influenza virus gene expression: control mechanisms at early and late times of infection and nuclear-cytoplasmic transport of virus-specific RNAs, J. Virol., 61, 764, 10.1128/jvi.61.3.764-773.1987 Shaw, 2008, Cellular proteins in influenza virus particles, PLoS Pathog., 4, 10.1371/journal.ppat.1000085 Sjöholm, 2017, Targeted proteomics and absolute protein quantification for the construction of a stoichiometric host-pathogen surface density model, Mol. Cell. Proteomics, 16, S29, 10.1074/mcp.M116.063966 Skehel, 2000, Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin, Annu. Rev. Biochem., 69, 531, 10.1146/annurev.biochem.69.1.531 Takashita, 2016, Influenza A(H1N1)pdm09 virus exhibiting enhanced cross-resistance to oseltamivir and peramivir due to a dual H275Y/G147R substitution, Japan, March 2016, Euro Surveill, 21, 10.2807/1560-7917.ES.2016.21.24.30258 Tapia, 2016, Bioreactors for high cell density and continuous multi-stage cultivations: options for process intensification in cell culture-based viral vaccine production, Appl. Microbiol. Biotechnol., 100, 2121, 10.1007/s00253-015-7267-9 Tapia, 2014, Production of high-titer human influenza A virus with adherent and suspension MDCK cells cultured in a single-use hollow fiber bioreactor, Vaccine, 32, 1003, 10.1016/j.vaccine.2013.11.044 Thrash, 1991, Effect of divalent ions on protein precipitation with polyethylene glycol: mechanism of action and applications, Protein Expr. Purif., 2, 83, 10.1016/1046-5928(91)90015-B Tian, 2004, Integrated genomic and proteomic analyses of gene expression in mammalian cells, Mol. Cell. Proteomics, 3, 960, 10.1074/mcp.M400055-MCP200 Trötschel, 2015, Current approaches and challenges in targeted absolute quantification of membrane proteins, Proteomics, 15, 915, 10.1002/pmic.201400427 Ward, 2004, Design and performance testing of quantitative real time PCR assays for influenza A and B viral load measurement, J. Clin. Virol., 29, 179, 10.1016/S1386-6532(03)00122-7