Correction: Analyzing clonal variation of monoclonal antibody-producing CHO cell lines using an in silico metabolomic platform (PLoS ONE (2014) 9, 3 (e90832) DOI: 10.1371/journal.pone.0090832);Analyzing clonal variation of monoclonal antibody-producing CHO cell lines using an in silico metabolomic platform

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Ghorbaniaghdam, Atefeh ^a   Chen, Jingkui ^a   Henry, Olivier ^a   Jolicoeur, Mario ^a  

^a ÉCOLE POLYTECHNIQUE DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; GLUTAMATE DEHYDROGENASE; GLUTAMIC ACID; MALATE DEHYDROGENASE (DECARBOXYLATING); OXALOACETIC ACID; PYRUVATE CARBOXYLASE; PYRUVATE DEHYDROGENASE; ALPHA-KETOGLUTARIC ACID; MONOCLONAL ANTIBODY; PYRUVATE DECARBOXYLASE; PYRUVIC ACID;

ANAPLEROSIS; ANIMAL CELL; ARTICLE; CATAPLEROSIS; CELL CLONE; CELL METABOLISM; CHEMICAL REACTION; CHO CELL; CITRIC ACID CYCLE; CLONAL VARIATION; COMPUTER MODEL; COMPUTER SIMULATION; CONTROLLED STUDY; GENE EXPRESSION; GENE SWITCHING; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; INTRACELLULAR TRANSPORT; METABOLIC REGULATION; NONHUMAN; OXIDATION REDUCTION STATE; PROTEIN TRANSPORT; ANIMAL; CHO CELL LINE; CRICETULUS; METABOLISM; METABOLOMICS; PHYSIOLOGY; PROCEDURES; THEORETICAL MODEL;

ANIMALS; ANTIBODIES, MONOCLONAL; CHO CELLS; CITRIC ACID CYCLE; CRICETULUS; KETOGLUTARIC ACIDS; METABOLOMICS; MODELS, THEORETICAL; PYRUVATE DECARBOXYLASE; PYRUVIC ACID;

EID: 84898483881     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104725     Document Type: Erratum

References (76)

1. Pavlou AK, Belsey MJ (2008) The therapeutic antibodies market to 2008. European Journal of Pharmaceutics and Biopharmceutics 59: 389-96. (Pubitemid 40342513)
2. Durocher Y, Butler M (2009) Expression systems for therapeutic glycoprotein production. Current Opinion in Biotechnology 20: 700-707.
3. Bebbington CR, Renner G, Thomson S, King D, Abrams D, et al. (1992) High-level expression of a recombinant antibody from myeloma cells using a glutamine synthetase gene as an amplifiable selectable marker. Biotechnology (NY) 10: 169-175.
4. Lee YY, Wong KT, Tan J, Toh PC, Mao Y, et al. (2009) Overexpression of heat shock proteins (HSPs) in CHO cells for extended culture viability and improved recombinant protein production. Journal of Biotechnology 143: 34-43.
5. Bi JX, Shuttleworth J, Al-Rubeai M (2004) Uncoupling of cell growth and proliferation results in enhancement of productivity in p21CIP1-arrested CHO cells. Biotechnology and Bioengineering 85: 741-749. (Pubitemid 38332410)
6. Eppink MHM, Schreurs R, Gusen A, Verhoeven K (2009) Platform technology for developing purification processes. Biopharm International Supplements March 2009: 32-36.
7. Shukla AA, Hubbard B, Tressel T, Guhan S, Low D (2007) Downstream processing of monoclonal antibodies - application of platform approaches. Journal of Chromatography B 848: 28-39. (Pubitemid 46367766)
8. Li F, Vijayasankaran N, Shen AY, Kiss R, Amanullah A (2010) Cell culture processes for monoclonal antibody production. mAbs Journal 2: 466-79.
9. Clarke GD (1965) Variations in the tumour-forming capacity of a line of rat fibroblasts (16C) following selection in vitro. British Journal of Cancer 19: 840-854.
10. Peterson JA (1976) Clonal variation in albumin messenger RNA activity in hepatoma cells. Proceedings of the National Academy of Sciences 6: 2056-2060.
11. Smales CM, Dinnis DM, Stansfield SH, Alete D, Sage EA, et al. (2004) Comparative proteomic analysis of GS-NS0 murine myeloma cell lines with varying recombinant monoclonal antibody production rate. Biotechnology and Bioengineering 88: 474-88. (Pubitemid 39536549)
12. Seth G, Philp RJ, Lau A, Jiun KY, Yap M, et al. (2007) Molecular portrait of high productivity in recombinant NS0 cells. Biotechnology and Bioengineering 97: 933-51. (Pubitemid 47051062)
13. Alete DE, Racher AJ, Birch JR, Stansfield SH, James DC, et al. (2005) Proteomic analysis of enriched microsomal fractions from GS-NS0 murine myeloma cells with varying secreted recombinant monoclonal antibody productivities. Proteomics 5: 4689-704. (Pubitemid 43016891)
14. Oh MK, Scoles DR, Haipek C, Strand AD, Gutmann DH, et al. (2003) Genetic heterogeneity of stably transfected cell lines revealed by expression profiling with oligonucleotide microarrays. Journal of Cell Biochemistry 90: 1068-1078. (Pubitemid 37467121)
15. Konrad MW, Storrie B, Glaser DA, Thompson LH (1977) Clonal variation in colony morphology and growth of CHO cells cultures on agar. Cell 10: 305-312. (Pubitemid 8056272)
16. Zdzienicka M, Cupido M, Simons JW (1985) Increase in clonal variation in Chinese hamster ovary cells after treatment with mutagens. Somatic Cells and Molecular Genetics 11: 127-134. (Pubitemid 15149286)
17. Kim NS, Byun TH, Lee GM (2001) Key determinants in the occurrence of clonal variation in humanized antibody expression of CHO cells during dihydrofolate reductase mediated gene amplification. Biotechnology Progress 17: 69-75.
18. Hayduk EJ, Choe LH, Lee KH (2004) A two dimentional electrophoresis map of Chinese hamster ovary cell proteins based on fluorescence staining. Electrophoresis 25: 2545-2556. (Pubitemid 39193665)
19. Hayduk EJ, Lee KH (2005) Cytochalasin D can improve heterologous protein productivity in adherent Chinese hamster ovary cells. Biotechnology and Bioengineering 90: 354-364. (Pubitemid 40779212)
20. Nissom PM, Sanny A, Kok YJ, Hiang YT, Chuah SH, et al. (2006) Transcriptome and proteome profiling to understanding the biology of high productivity CHO cells. Molecular Biotechnology 34: 125-140. (Pubitemid 46030386)
21. Chusainow J, Yang YS, Yeo JH, Toh PC, Asvadi P, et al. (2009) A study of monoclonal antibody-producing CHO cell lines: what makes a stable high producer? Biotechnology and Bioengineering 102: 1182-1196.
22. Davies SL, Lovelady CS, Grainger RK, Racher AJ, Young RJ, et al. (2012) Functional heterogeneity and heritability in CHO cell populations. Biotechnology and Bioengineering 110: 260-274.
23. Yoon SK, Hwang SO, Lee GM (2004) Enhancing effect of low culture temperature on specific antibody productivity of recombinant Chinese hamster ovary cells: clonal variation. Biotechnology Progress 20: 1683-1688.
24. Dahodwala H, Nowey M, Mitina T, Sharfstein ST (2012) Effect of clonal variation in growth, metabolism, and productivity in response to trophic factor stimulation: a study of Chinese hamster ovary cells. Cytotechnology 64: 27-41.
25. Mo ML, Palsson BO, Herrgård MJ (2009) Connecting extracellular metabolomic measurements to intracellular flux states in yeast BMC Systems Biology 25: 3-37.
26. Metallo CM, Walther JL, Stephanopoulos G (2009) Evaluation of 13C isotopic tracers for metabolic flux analysis in mammalian cells. Journal of Biotechnology 144: 167-174.
27. Ahn WC, Antoniewicz MR (2011) Metabolic flux analysis of CHO cells at growth and non-growth phases using isotopic tracers and mass spectrometry. Metabolic Engineering 13: 598-609.
28. Templeton N, Dean J, Reddy P, Young JD (2013) Peak antibody production is associated with increased oxidative metabolism in an industrially relevant fed-batch CHO cell culture. Biotechnology and Bioengineering 110: 2013-2014.
29. Sheikholeslami Z, Jolicoeur M, Henry O (2013) Probing the metabolism of an inducible mammalian expression system using extracellular isotopomer analysis. Journal of Biotechnology 164: 496-478.
30. Dean J, Reddy PV (2013) Metabolic Analysis of Antibody Producing CHO Cells in Fed-Batch Production. Biotechnology and Bioengineering 110: 1735-1747.
31. Zamorano F, Vande Wouwer A, Jungers RM, Bastin G (2012) Dynamic metabolic models of CHO cell cultures through minimal sets of elementary flux modes. Journal of Biotechnology 146: 409-422.
32. Dorka P, Fischer C, Budman H, Scharer JM (2009) Metabolic flux-based modeling of mAb production during batch and fed-batch operations. Bioprocess and Biosystems Engineering 32: 183-196.
33. Naderi S, Meshram M, Wei C, McConkey B, Ingalls B, et al. (2011) Development of a mathematical model for evaluating the dynamics of normal and apoptotic Chinese hamster ovary cells. Biotechnology Progress 27: 1197-1205.
34. Nolan RP, Lee K (2011) Dynamic model of CHO cell metabolism. Metab Eng 13: 108-124.
35. Zomorrodi AR, Suthers PF, Ranganathan S, Maranas CD (2012) Mathematical optimization applications in metabolic networks. Metabolic Engineering 14: 672-686.
36. Ghorbaniaghdam A, Henry O, Jolicoeur M (2012) A kinetic-metabolic model based on cell energetic state: study of CHO cell behavior under Na-butyrate stimulation. Bioprocess and Biosystems Engineering 36: 469-487.
37. Mullick A, Xu Y, Warren R, Koutroumanis M, Guilbault C, et al. (2006) The cumate gene-switch: a system for regulated expression in mammalian cells. BMC Biotechnology 6 : 43-61.
38. Gaillet B, Gilbert R, Broussau S, Pilotte A, Malenfant F, et al. (2010) High-level recombinant protein production in CHO cells using lentiviral vectors and the cumate gene-switch. Biotechnology and Bioengineering 106, 203-215.
39. Preinerstorfer B, Schiesel S, Lämmerhofer M, Lindner W (2010) Metabolic profiling of intracellular metabolites in fermentation broths from β-lactam antibiotics production by liquid chromatography-tandem mass spectrometry methods. Journal of Chromatography A 1217: 312-328.
40. Dell'mour M, Jaitz L, Oburger E, Puschenreiter M, Koellensperger G, et al. (2010) Hydrophilic interaction LC combined with electrospray MS for highly sensitive analysis of underivatized amino acids in rhizosphere research. Journal of Separation Science 33: 911-922.
41. Lamboursain L, St-Onge F, Jolicoeur M (2002) A lab-respirometer for plant and animal cell culture. Biotechnology Progress 8: 1377-1386. (Pubitemid 35450897)
42. Qian T, Cai Z, Yang MS (2004) Determination of adenosine nucleotides in cultured cells by ion-pairing liquid chromatography-electrospray ionization, mass spectrometry. Analytical Biochemistry 325: 77-84. (Pubitemid 38050269)
43. Pugin A, Frachisse JM, Tavernier E, Bligny R, Gout E, et al. (1997) Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxydase and activation of glycolysis and the pentose phosphate pathway, The Plant Cell 9: 2077-2091. (Pubitemid 28174078)
44. 31 P NMR, Comparative Biochemistry and Physiology Cart C 140: 103-113.
45. Martens DE (2007) Metabolic Flux Analysis of Mammalian Cells, in : Cell Engineering Volume 5. M. Al-Rubeai and M. Fussenegger Eds. pp. 275-299.
46. Segel IH (1993) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, Wiley Classic Library. ISBN 0-471-30309-7
47. Atkinson DE (1968) Energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7: 4030-4034.
48. Scheer M, Grote A, Chang A, Schomburg I, Munaretto C, et al. (2011) BRENDA, the enzyme information system. Nucleic Acids Research. 39(Database issue http://www.brenda-enzymes.org/)): D670-676.
49. Hardie DG, Hawley SA (2001) AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays 23: 1112-1119.
50. Stephanopoulos G, Aristodou A, Nielsen J (1998) Metabolic Engineering. Principles and Methodologies: Academic Press, San Diego.
51. Dash RK, Li Y, Kim J, Saidel GM, Cabrera ME (2008) Modeling Cellular Metabolism and Energetics in Skeletal Muscle: Large-Scale Parameter Estimation and Sensitivity Analysis. IEEE Transactions on Biomedical Engineering 55: 1298-1318. (Pubitemid 351440496)
52. Hundal HS, Rennie MJ, Watt PW (1989) Characteristics of acidic, basic and neutral amino acid transport in the perfused rat hindlimb. Journal of Physiology 408: 93-114. (Pubitemid 19040011)
53. Liebermeister W, Klipp E (2006) Bringing metabolic networks to life: convenience rate law and thermodynamic constraints. Theoretical Biology and Medical Modeling 3: 41-54.
54. th Edition. WH Freeman Eds. New-York.
55. Garreau H, Buc-Temkine H (1972) Allosteric activation of human erythrocyte pyruvate kinase by fructose-1,6-diphosphate: Kinetic and equilibrium binding studies. Biochimie 54: 1103-1107.
56. Wang CS (1977) Inhibition of human erythrocyte lactate dehydrogenase by high concentrations of pyruvate. Evidence for the competitive substrate inhibition. European Journal of Biochemistry 78: 569-574.
57. Heinrich R, Rapoport SM (1977) Metabolic regulation and mathematical models. Progress in Biophysics and Molecular Biology 32: 1-82. (Pubitemid 8124824)
58. Reich JG, Selkov EE (1981) Energy metabolism of the cell - a theoritical treatise. London: Academic Press. 645p.
59. Mailier J, Delmotte A, Cloutier M, Jolicoeur M, Vande Wouwer A (2011) Parametric sensitivity analysis and reduction of a detailed nutritional model of plant cell cultures. Biotechnology and Bioengineering 108: 1108-1118.
60. Zagari F, Jordan M, Stettler M, Broly H, Wurm FM (2013) Lactate metabolism shift in CHO cell culture: the role of mitochondrial oxidative activity. Nature Biotechnology 30: 238-245.
61. Heyland J, Blank LM, Schmid A (2011a) Quantification of metabolic limitations during recombinant protein production in Escherichia coli. Journal of Biotechnology 155: 178-184.
62. Heyland J, Fu J, Blank LM, Schmid A (2011b) Carbon metabolism limits recombinant protein production in Pichia pastoris. Biotechnology and Bioengineering 108: 1942-1953.
63. Dinnis DM, Stansfield SH, Schlatter S, Smales CM, Alete D, et al. (2006) Functional proteomic analysis of GS-NS0 murine myeloma cell lines with varying recombinant monoclonal antibody production rate. Biotechnology and Bioengineering 94: 830-841. (Pubitemid 44186891)
64. Europa AF, Gambhir A, Fu PC, Hu WS (2006) Multiple steady states with distinct cellular metabolism in continuous culture of mammalian cells. Biotechnology and Bioengineering 67: 25-34.
65. Lehninger AL (1977) Biochemistry. Worth, New York; 1104 p.
66. Irani N, Beccaria AJ, Wagner R (2002) Expression of recombinant cytoplasmic yeast pyruvate carboxylase for the improvement of the production of human erythropoietin by recombinant BHK-21 cells. Biotechnology 93: 269-82. (Pubitemid 34084860)
67. Fogolín MB, Wagner R, Etcheverrigaray M, Kratje R (2004) Impact of temperature reduction and expression of yeast pyruvate carboxylase on hGM-CSF-producing CHO cells. Biotechnology 109: 179-191. (Pubitemid 38452583)
68. Altamirano C, Illanes A, Casablancas A, Gamez X, Cairo JJ, et al. (2001) Analysis of CHO cells metabolic redistribution in a glutamate-based defined medium in continuous culture. Biotechnology Progress 17: 1032-1041. (Pubitemid 34018281)
69. Goudar C, Biener R, Boisart C, Heidemann R, Piret J, et al. (2010) Metabolic flux analysis of CHO cells in perfusion culture by metabolite balancing and 2D[13C,1H] COSYNMR spectroscopy. Metabolic Engineering 12: 138-149.
70. Sengupta N, Rose ST, Morgan JA (2011) Metabolic Flux Analysis of CHO Cell Metabolism in the Late Non-Growth Phase. Biotechnol and Bioeng 108: 82-92.
71. Niklas J, Schräder E, Sandig V, Noll T, Heinzle E (2011) Quantitative characterization of metabolism and metabolic shifts during growth of the new human cell line AGE1.HN using time resolved metabolic flux analysis. Bioprocess and Biosystems Engineering 34: 533-545.
72. Bonarius HP, Houtman JH, de Gooijer CD, Tramper J, Schmid G (1998) Activity of glutamate dehydrogenase is increased in ammonia-stressed hybridoma cells. Biotechnology and Bioengineering 57: 447-453. (Pubitemid 28051553)
73. Beard DA (2006) Modeling of oxygen transport and cellular energetics explains observations on in vivo cardiac energy metabolism. PLoS Computational Biology 2: 1093-1097.
74. Harper ME, Antoniou A, Bevilacqua L, Bezaire V, Monemdjou S (2002) Cellular energy expenditure and the importance of uncoupling. Journal of Animal Science 80: 90-97.
75. Link T, Backstrom M, Graham R, Essers R, Zorner K, et al. (2004) Bioprocess development for the production of a recombinant MUC1 fusion protein expressed by CHO-K1 cells in protein-free medium. Journal of Biotechnology 110: 51-62. (Pubitemid 38510253)
76. Chong WPK, Thng SH, Hiu AP, Lee DY, Chan ECY, et al. (2012) LC-MS-Based Metabolic Characterization of High Monoclonal Antibody-Producing Chinese Hamster Ovary Cells. Biotechnologyogy and Bioengineering 109: 3103-3111.