Influence of HEK293 metabolism on the production of viral vectors and vaccine

Vaccine

Volumn 33, Issue 44, 2015, Pages 5974-5981

  Petiot, Emma ^a   Cuperlovic Culf, Miroslava ^b   Shen, Chun Fang ^b   Kamen, Amine ^b,c  

^a UNIVERSITÉ LYON 1   (France)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

HEK293 cell metabolism; Metabolomics; Viral production processes; Viral vector and vaccine

Indexed keywords

RECOMBINANT PROTEIN; VIRUS VACCINE; VIRUS VECTOR; DRUG CARRIER; VACCINE;

AEROBIC METABOLISM; AMINO ACID METABOLISM; AMMONIA FORMATION; ARTICLE; BIOSYNTHESIS; CARBON SOURCE; CELL CULTURE; CELL DENSITY; CELL ENGINEERING; CELL METABOLISM; CITRIC ACID CYCLE; EMBRYO; ENERGY METABOLISM; GLYCOLYSIS; HEK293 CELL LINE; HUMAN; HUMAN CELL; MAMMAL CELL; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; TRANSIENT EXPRESSION; VACCINE PRODUCTION; CELL CULTURE TECHNIQUE; CELL LINE; EPITHELIUM CELL; ISOLATION AND PURIFICATION; METABOLISM; PHARMACEUTICS;

CELL CULTURE TECHNIQUES; CELL LINE; DRUG CARRIERS; EPITHELIAL CELLS; HUMANS; TECHNOLOGY, PHARMACEUTICAL; VACCINES;

EID: 84947489141     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.05.097     Document Type: Article

References (91)

1. Nadeau I., Kamen A. Production of adenovirus vector for gene therapy. Biotechnol Adv 2003, 20:475-489.
2. Fontana D., Kratje R., Etcheverrigaray M., Prieto C. Rabies virus-like particles expressed in HEK293 cells. Vaccine 2014, 32:2799-2804.
3. Petiot E., Kamen A.A., Emma P. Real-time monitoring of influenza virus production kinetics in HEK293 cell cultures. Biotechnol Prog 2012, 29.
4. Pham P.L., Perret S., Doan H.C., Cass B., St-Laurent G., Kamen A., et al. Large-scale transient transfection of serum-free suspension-growing HEK293 EBNA1 cells: peptone additives improve cell growth and transfection efficiency. Biotechnol Bioeng 2003, 84:332-342.
5. Rodrigues a F., Formas-Oliveira a S., Bandeira V.S., Alves P.M., Hu W.S., Coroadinha A.S. Metabolic pathways recruited in the production of a recombinant enveloped virus: mining targets for process and cell engineering. Metab Eng 2013, 20:131-145.
6. Butler M., Spearman M. The choice of mammalina cell host and possibilities for glycosylation engineering. Curr Opin Biotechol 2014, 30:107-112.
7. Swiech K., Picanço-Castro V., Covas D.T. Human cells: new platform for recombinant therapeutic protein production. Protein Exp Purif 2012, 84:147-153.
8. Rodrigues A.F., Carrondo M.J.T., Alves P.M., Coroadinha A.S. Cellular targets for improved manufacturing of virus-based biopharmaceuticals in animal cells. Trends Biotechnol 2014, 32:602-607.
9. Cuperlović-Culf M., Barnett D.A., Culf A.S., Chute I. Cell culture metabolomics: applications and future directions. Drug Discovery Today 2010, 15:610-621.
10. Khoo S.H.G., Al-Rubeai M. Metabolomics as a complementary tool in cell culture. Biotechnol Appl Biochem 2007, 47:71-84.
11. Griffin J. Metabonomics NMR spectroscopy and pattern recognition analysis of body fluids and tissues for characterisation of xenobiotic toxicity and disease diagnosis. Curr Opin Chem Biol 2003, 7:648-654.
12. Paglia G., Hrafnsdóttir S., Magnúsdóttir M., Fleming R.M.T., Thorlacius S., Palsson B.Ø., et al. Monitoring metabolites consumption and secretion in cultured cells using ultra-performance liquid chromatography quadrupole-time of flight mass spectrometry (UPLC-Q-ToF-MS). Anal Bioanal Chem 2012, 402:1183-1198.
13. Quek L-E., Dietmair S., Krömer J.O., Nielsen L.K. Metabolic flux analysis in mammalian cell culture. Metab Eng 2010, 12:161-171.
14. Tomar N., De R.K. Comparing methods for metabolic network analysis and an application to metabolic engineering. Gene 2013, 521:1-14.
15. Orth J.D., Thiele I., Palsson B.Ø. What is flux balance analysis?. Nat Biotechnol 2010, 28:245-248.
16. Hörl M., Schnidder J., Sauer U., Zamboni N. Non-stationary (13)C-metabolic flux ratio analysis. Biotechnol Bioeng 2013, 110:3164-3176. (d).
17. Iwatani S., Yamada Y., Usuda Y. Metabolic flux analysis in biotechnology processes. Biotechnol Lett 2008, 30:791-799.
18. Wegner A., Meiser J., Weindl D., Hiller K. How metabolites modulate metabolic flux. Curr Opin Biotechnol 2015, 34:16-22.
19. Buescher J.M., Antoniewicz M.R., Boros L.G., Burgess S.C., Brunengraber H., Clish C.B., et al. A roadmap for interpreting 13C metabolite labeling patterns from cells. Curr Opin Biotechnol 2015, 34:189-201.
20. Oldiges M., Lütz S., Pflug S., Schroer K., Stein N., Wiendahl C. Metabolomics: current state and evolving methodologies and tools. Appl Microbiol Biotechnol 2007, 76:495-511.
21. Patti G.J., Yanes O., Siuzdak G. Innovation Metabolomics: the apogee of the omics trilogy. Nat Rev Mol Cell Biol 2012, 13:263-269.
22. Winter G., Krömer J.O. Fluxomics-connecting' omics analysis and phenotypes. Environ Microbiol 2013, 15:1901-1916.
23. Gomez-Cabrero D., Abugessaisa I., Maier D., Teschendorff A., Merkenschlager M., Gisel A., et al. Data integration in the era of omics: current and future challenges. BMC Syst Biol 2014, 8:I1.
24. Joyce A.R., Palsson B.O. The model organism as a system: integrating omics data sets. Nat Rev Mol Cell Biol 2006, 7:198-210.
25. Munger J., Bajad S.U., Coller Ha, Shenk T., Rabinowitz J.D. Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathog 2006, 2:e132.
26. Kamen A., Henry O. Development and optimization of an adenovirus production process. J Gene Med 2004, 6:S184-S192.
27. Diamond D.L., Syder A.J., Jacobs J.M., Sorensen C.M., Walters K.A., Proll S.C., et al. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog 2010, 6:e1000719.
28. Delgado T., Sanchez E.L., Camarda R., Lagunoff M. Global metabolic profiling of infection by an oncogenic virus: KSHV induces and requires lipogenesis for survival of latent infection. PLoS Pathog 2012, 8:e1002866.
29. Dietmair S., Hodson M.P., Quek L-E., Timmins N.E., Gray P., Nielsen L.K. A multi-omics analysis of recombinant protein production in Hek293 cells. PLoS ONE 2012, 7:e43394.
30. Bardeletti G., Henry M., Sohier R., Gautheron D. Primary effects of the rubella virus on the metabolism of BHK-21 cells grown in suspension cultures. Arch Gesamte Virusforsch 1972, 39:26-34.
31. Vaheri A., Cristofalo V.J. Metabolism of rubella virus-infected BHK 21 cells. Enhanced glycolysis and late cellular inhibition. Arch Gesamte Virusforsch 1967, 21:425-436.
32. Bardeletti G. Respiration and ATP level in BHK21-13S cells during earliest stages of Rubella-virus replication. Intervirology 1977, 8:100-109.
33. Munger J., Bennett B.D., Parikh A., Feng X.J., McArdle J., Rabitz H.A., et al. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat Biotechnol 2008, 26:1179-1186.
34. El-Bacha T., Menezes M.M., Azevedo e Silva M.C., Sola-Penna M., Da Poian A.T. Mayaro virus infection alters glucose metabolism in cultured cells through activation of the enzyme 6-phosphofructo 1-kinase. Mol Cell Biochem 2004, 266:191-198.
35. El-Bacha T., Midlej V., Pereira da Silva A.P., Silva da Costa L., Benchimol M., Galina A., et al. Mitochondrial and bioenergetic dysfunction in human hepatic cells infected with dengue 2 virus. Biochim Biophys Acta 2007, 1772:1158-1166.
36. Green M., Henle G., Deinhardt F. Respiration and glycolysis of human cells grown in tissue culture. Virology 1958, 5:206-219.
37. Baron S., Levy H.B. Some metabolic effects of poliomyelitis virus on tissue culture. Nature 1956, 178:1230-1231.
38. Salzman N.P., Lockart R.Z., Sebring E.D. Alterations in HeLa cell metabolism resulting from poliovirus infection. Virology 1959, 9:244-259.
39. Levy H.B., Baron S. The effect of animal viruses on host cell metabolism. II. Effect of poliomyelitis virus on glycolysis and uptake of glycine by monkey kidney tissue cultures. J Infect Dis 1957, 100:109-118.
40. Burgener A., Coombs K., Butler M. Intracellular ATP and total adenylate concentrations are critical predictors of reovirus productivity from Vero cells. Biotechnol Bioeng 2006, 94:667-679.
41. Klemperer H. Glucose breakdown in chick embryo cells infected with influenza virus. Virology 1961, 13:68-77.
42. Thiele I., Swainston N., Fleming R.M.T., Hoppe A., Sahoo S., Aurich M.K., et al. A community-driven global reconstruction of human metabolism. Nat Biotechnol 2013, 31:419-425.
43. Quek L.-E., Dietmair S., Hanscho M., Martínez V.S., Borth N., Nielsen L.K. Reducing Recon 2 for steady-state flux analysis of HEK cell culture. J Biotechnol 2014, 184:172-178.
44. Nadeau I., Sabatié J., Koehl M., Perrier M., Kamen a. Human 293 cell metabolism in low glutamine-supplied culture: interpretation of metabolic changes through metabolic flux analysis. Metab Eng 2000, 2:277-292.
45. Lee Y.Y., Yap M.G.S., Hu W-S., Wong K.T.K. Low-glutamine fed-batch cultures of 293-HEK serum-free suspension cells for adenovirus production. Biotechnol Prog 2003, 19:501-509.
46. Henry O., Jolicoeur M., Kamen A. Unraveling the metabolism of HEK-293 cells using lactate isotopomer analysis. Bioprocess Biosyst Eng 2011, 34:263-273.
47. Nadeau I., Gilbert P.A., Jacob D., Perrier M., Kamen A. Low-protein medium affects the 293SF central metabolism during growth and infection with adenovirus. Biotechnol Bioeng 2002, 77:91-104.
48. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
49. Tennant D.a., Durán R.V., Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 2010, 10:267-277.
50. Martinez V., Gerdtzen Z.P., Andrews B.A., Asenjo J.A. Viral vectors for the treatment of alcoholism: use of metabolic flux analysis for cell cultivation and vector production. Metab Eng 2010, 12:129-137.
51. Nadeau I., Jacob D., Perrier M., Kamen A. 293SF metabolic flux analysis during cell growth and infection with an adenoviral vector. Biotechnol Prog 2000, 16:872-874.
52. Molinas M de los M.B. Transient transfection of HEK293 cells in suspension: process characterization and optimization by applying invasive nucleotide and non-invasive electronic nose technology 2005, (Doctoral thesis). http://d-nb.info/976524295/34.
53. Mulukutla B.C., Gramer M., Hu W-S. On metabolic shift to lactate consumption in fed-batch culture of mammalian cells. Metab Eng 2012, 14:138-149.
54. Martínez V.S., Dietmair S., Quek L-E., Hodson M.P., Gray P., Nielsen L.K. Flux balance analysis of CHO cells before and after a metabolic switch from lactate production to consumption. Biotechnol Bioeng 2013, 110:660-666.
55. Sonveaux P., Végran F., Schroeder T., Wergin M.C., Verrax J., Rabbani Z.N., et al. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 2008, 118:3930-3942.
56. Zagari F., Jordan M., Stettler M., Broly H., Wurm F.M. Lactate metabolism shift in CHO cell culture: the role of mitochondrial oxidative activity. Nat Biotechnol 2013, 30:238-245.
57. Henry O., Durocher Y. Enhanced glycoprotein production in HEK-293 cells expressing pyruvate carboxylase. Metab Eng 2011, 13:499-507.
58. Le Ru A., Jacob D., Transfiguracion J., Ansorge S., Henry O., Kamen A.A. Scalable production of influenza virus in HEK-293 cells for efficient vaccine manufacturing. Vaccine 2010, 28:3661-3671.
59. Elias C.B., Carpentier E., Durocher Y., Bisson L., Wagner R., Kamen A. Improving glucose and glutamine metabolism of human HEK 293 and Trichoplusia ni insect cells engineered to express a cytosolic pyruvate carboxylase enzyme. Biotechnol Prog 2003, 19:90-97.
60. Cervera L., Gutiérrez-Granados S., Martínez M., Blanco J., Gòdia F., Segura M.M. Generation of HIV-1 Gag VLPs by transient transfection of HEK 293 suspension cell cultures using an optimized animal-derived component free medium. J Biotechnol 2013, 166:152-165.
61. Ferreira T.B., Carrondo M.J.T., Alves P.M. Effect of ammonia production on intracellular pH: consequent effect on adenovirus vector production. J Biotechnol 2007, 129:433-438.
62. Cruz H.J., Freitas C.M., Alves P.M., Moreira J.L., Carrondo M.J.T. Effects of ammonia and lactate on growth, metabolism, and productivity of BHK cells. Enzyme Microb Technol 2000, 27:43-52.
63. Pham P.L., Perret S., Cass B., Carpentier E., St-Laurent G., Bisson L., et al. Transient gene expression in HEK293 cells: peptone addition posttransfection improves recombinant protein synthesis. Biotechnol Bioeng 2005, 90:332-344.
64. Petiot E., Jacob D., Lanthier S., Lohr V., Ansorge S., Kamen A.A. Metabolic and kinetic analyses of influenza production in perfusion HEK293 cell culture. BMC Biotechnol 2011, 11:84.
65. Ferreira T.B., Ferreira a L., Carrondo M.J.T., Alves P.M. Effect of re-feed strategies and non-ammoniagenic medium on adenovirus production at high cell densities. J Biotechnol 2005, 119:272-280.
66. Rodrigues A.F., Carmo M., Alves P.M., Coroadinha a.S. Retroviral vector production under serum deprivation: the role of lipids. Biotechnol Bioeng 2009, 104:1171-1181.
67. Carinhas N., Bernal V., Yokomizo A.Y., Carrondo M.J.T., Oliveira R., Alves P.M. Baculovirus production for gene therapy: the role of cell density, multiplicity of infection and medium exchange. Appl Microbiol Biotechnol 2009, 81:1041-1049.
68. Liu X., Zhao L., Wang Y., Zhang X., Tan W-S. Effects of calcium ion on adenovirus production with high densities of HEK293 cells. Biotechnol Bioprocess Eng 2010, 15:414-420.
69. Bernal V., Carinhas N., Yokomizo A.Y., Carrondo M.J.T., Alves P.M. Cell density effect in the baculovirus-insect cells system: a quantitative analysis of energetic metabolism. Biotechnol Bioeng 2009, 104:162-180.
70. Kamen A., Henry O. Development and optimization of an adenovirus production process. J Gene Med 2004, 6(Suppl. 1):S184-S192.
71. Gálvez J., Lecina M., Solà C., Cairó J.J., Gòdia F. Optimization of HEK-293S cell cultures for the production of adenoviral vectors in bioreactors using on-line OUR measurements. J Biotechnol 2012, 157:214-222.
72. Bereheiter-Hahn J., Munnich A., Woiteneck P. Dependence of energy metabolism on the density of cells in culture. Cell Struct Funct 1998, 23:85-93.
73. Bar J., Cohen-Noyman E., Geiger B., Oren M. Attenuation of the p53 response to DNA damage at high cell density. Oncogene 2004, 23:2128-2137.
74. Vukelic Z., Kalanj-Bognar S. Cell density-dependent changes of glycosphingolipid biosynthesis in cultured human skin fibroblasts. Glycoconjugate J 2001, 18:429-437.
75. Shen C.F., Voyer R., Tom R., Kamen A. Reassessing culture media and critical metabolites that affect adenovirus production. Biotechnol Prog 2010, 26:200-207.
76. Ferreira T.B., Perdigão R., Silva A.C., Zhang C., Aunins J.G., Carrondo M.J.T., et al. 293 Cell cycle synchronisation in adenovirus vector production. Biotechnol Prog 2009, 25:235-243.
77. Feuer R., Mena I., Pagarigan R., Slifka M.K., Whitton J.L. Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J Virol 2002, 76:4430-4440.
78. Liste-Calleja L., Lecina M., Cairó J.J. HEK293 cell culture media study towards bioprocess optimization: animal derived component free and animal derived component containing platforms. J Biosci Bioeng 2014, 117:471-477.
79. Cervera L., Gutiérrez S., Gòdia F., Segura M.M. Optimization of HEK 293 cell growth by addition of non-animal derived components using design of experiments. BMC Proc 2011, 5(Suppl. 8):P126.
80. Shen C.F., Lanthier S., Jacob D., Montes J., Beath A., Beresford A., et al. Process optimization and scale-up for production of rabies vaccine live adenovirus vector (AdRG1.3). Vaccine 2012, 30:300-306.
81. Shen C.F., Kamen A. Hyperosmotic pressure on HEK 293 cells during the growth phase, but not the production phase, improves adenovirus production. J Biotechnol 2012, 157:228-236.
82. Ansorge S., Lanthier S., Transfiguracion J., Henry O., Kamen A. Monitoring lentiviral vector production kinetics using online permittivity measurements. Biochem Eng J 2011, 54:16-25.
83. Merten O.W. State-of-the-art of the production of retroviral vectors. J Gene Med 2004, 6(Suppl. 1):S105-S124.
84. Mitta B., Rimann M., Fussenegger M. Detailed design and comparative analysis of protocols for optimized production of high-performance HIV-1-derived lentiviral particles. Metab Eng 2005, 7:426-436.
85. Rodrigues A.F., Alves P.M., Coroadinha A.S. Production of retroviral and lentiviral gene therapy vectors: challenges in the manufacturing of lipid enveloped virus. Viral gene therapy 2010, INTECH. K. Xu (Ed.).
86. Petiot E., Guedon E., Blanchard F., Geny C., Pinton H., Marc A., et al. Kinetic characterization of vero cell metabolism in a serum-free batch culture process. Biotechnol Bioeng 2010, 107:143-153.
87. Genzel Y., Ritter J.B., König S., Alt R., Reichl U. Substitution of glutamine by pyruvate to reduce ammonia formation and growth inhibition of mammalian cells. Biotechnol Prog 2005, 21:58-69.
88. Ferreira T., Carrondo M., Alves P. Effect of ammonia production on intracellular pH: consequent effect on adenovirus vector production. J Biotechnol 2007, 129:433-438.
89. Liu H., Liu X-M., Li S-C., Wu B-C., Ye L-L., Wang Q-W., et al. A high-yield and scaleable adenovirus vector production process based on high density perfusion culture of HEK 293 cells as suspended aggregates. J Biosci Bioeng 2009, 107:524-529.
90. Ghani K., Cottin S., Kamen A., Caruso M. Generation of a high-titer packaging cell line for the production of retroviral vectors in suspension and serum-free media. Gene Ther 2007, 14:1705-1711.
91. Ghani K., Wang X., de Campos-Lima P.O., Olszewska M., Kamen A., Rivière I., et al. Efficient human hematopoietic cell transduction using RD114- and GALV-pseudotyped retroviral vectors produced in suspension and serum-free media. Hum Gene Ther 2009, 20:966-974.