Metabolic adaptation of MDCK cells to different growth conditions: Effects on catalytic activities of central metabolic enzymes

Biotechnology and Bioengineering

Volumn 108, Issue 11, 2011, Pages 2691-2704

  Janke, R ^a   Genzel, Y ^a   Handel N ^b   Wahl, A ^c   Reichl, U ^a,d  

^a MAX PLANCK INSTITUTE FOR DYNAMICS OF COMPLEX TECHNICAL SYSTEMS   (Germany)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Enzymes; Glutaminolysis; Glycolysis; MDCK; Metabolic adaptation; Metabolism; Pyruvate

Indexed keywords

GLUTAMINOLYSIS; GLYCOLYSIS; MDCK; METABOLIC ADAPTATION; PYRUVATES;

AMINO ACIDS; AMMONIA; ANIMAL CELL CULTURE; CATALYST ACTIVITY; CELL GROWTH; CYTOLOGY; ENERGY MANAGEMENT; ENZYME ACTIVITY; ENZYMES; GLUCOSE; GROWTH KINETICS; LAKES; MAMMALS; METABOLISM; PHYSIOLOGY;

CELLS;

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GLUCOSE; GLUCOSE 6 PHOSPHATE; GLUTAMATE AMMONIA LIGASE; GLUTAMATE DEHYDROGENASE; GLUTAMINE; ISOCITRATE DEHYDROGENASE; PYRUVATE CARBOXYLASE; PYRUVATE DEHYDROGENASE; PYRUVIC ACID;

ADAPTATION; AMINO ACID METABOLISM; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL GROWTH; CELL METABOLISM; CELL STRAIN; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVITY; GLUCOSE METABOLISM; MAMMAL CELL; NONHUMAN; PENTOSE PHOSPHATE CYCLE; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE; DOGS; ENZYMES; EPITHELIAL CELLS; KIDNEY; METABOLIC NETWORKS AND PATHWAYS; STRESS, PHYSIOLOGICAL;

MAMMALIA;

EID: 80053052951     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.23215     Document Type: Article

References (58)

1. Ardawi MSM, Newsholme EA. 1982. Maximum activities of some enzymes of glycolysis, the tricarboxylic acid cycle and ketone body and glutamine utilization pathways in lymphocytes of the rat. Biochem J 208(3): 743-748.
2. Ardawi MSM, Newsholme EA. 1983. Glutamine metabolism in lymphocytes of the rat. Biochem J 212(3): 835-842.
3. Bell SL, Bebbington C, Scott MF, Wardell JN, Spier RE, Bushell ME, Sanders PG. 1995. Genetic engineering of hybridoma glutamine metabolism. Enzyme Microb Technol 17(2): 98-106.
4. Bock A, Schulze-Horsel J, Schwarzer J, Rapp E, Genzel Y, Reichl U. 2010. High-density microcarrier cell cultures for influenza virus production. Biotechnol Prog 27(1): 241-250.
5. Bonarius HPJ, Houtman JHM, de Gooijer CD, Tramper J, Schmid G. 1998. Activity of glutamate dehydrogenase is increased in ammonia-stressed hybridoma cells. Biotechnol Bioeng 57(4): 447-453.
6. Butler M, Christie A. 1994. Adaptation of mammalian cells to non-ammoniagenic media. Cytotechnology 15(1-3): 87-94.
7. Butler M, Spier RE. 1984. The effects of glutamine utilisation and ammonia production on the growth of BHK cells in microcarrier cultures. J Biotechnol 1(3-4): 187-196.
8. Carinhas N, Bernal V, Monteiro F, Carrondo MJ, Oliveira R, Alves PM. 2010. Improving baculovirus production at high cell density through manipulation of energy metabolism. Metab Eng 12(1): 39-52.
9. Christie A, Butler M. 1999. The adaptation of BHK cells to a non-ammoniagenic glutamate-based culture medium. Biotechnol Bioeng 64(3): 298-309.
10. Cruz HJ, Freitas CM, Alves PM, Moreira JL, Carrondo MJT. 2000. Effects of ammonia and lactate on growth, metabolism, and productivity of BHK cells. Enzyme Microb Technol 27(1-2): 43-52.
11. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S, Thompson CB. 2007. Beyond aerobic glycolysis: Transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci USA 104(49): 19345-19350.
12. DeBerardinis RJ, Sayed N, Ditsworth D, Thompson CB. 2008. Brick by brick: Metabolism and tumor cell growth. Curr Opin Genet Dev 18(1): 54-61.
13. (R) (Novartis Vaccines). Expert Rev Vaccines 8(6): 679-688.
14. Fell DA. 1998. Increasing the flux in metabolic pathways: A metabolic control analysis perspective. Biotechnol Bioeng 58(2-3): 121-124.
15. Fell DA, Thomas S. 1995. Physiological control of metabolic flux: The requirement for multisite modulation. Biochem J 311: 35-39.
16. Fitzpatrick L, Jenkins HA, Butler M. 1993. Glucose and glutamine metabolism of a murine B-lymphocyte hybridoma grown in batch culture. Appl Biochem Biotechnol 43(2): 93-116.
17. Genzel Y, Reichl U. 2009. Continuous cell lines as a production system for influenza vaccines. Expert Rev Vaccines 8(12): 1681-1692.
18. Genzel Y, Behrendt I, König S, Sann H, Reichl U. 2004a. Metabolism of MDCK cells during cell growth and influenza virus production in large-scale microcarrier culture. Vaccine 22(17-18): 2202-2208.
19. Genzel Y, König S, Reichl U. 2004b. Amino acid analysis in mammalian cell culture media containing serum and high glucose concentrations by anion exchange chromatography and integrated pulsed amperometric detection. Anal Biochem 335(1): 119-125.
20. Genzel Y, Ritter JB, König S, Alt R, Reichl U. 2005. Substitution of glutamine by pyruvate to reduce ammonia formation and growth inhibition of mammalian cells. Biotechnol Prog 21(1): 58-69.
21. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Höhne M, Hendriks JHM, Palacios N, Cross J, Selbig J, Stitt M. 2004. A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: Comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16(12): 3304-3325.
22. Glacken MW. 1988. Catabolic control of mammalian cell culture. Bio-Technology 6(9): 1041-1050.
23. Glacken MW, Fleischaker RJ, Sinskey AJ. 1986. Reduction of waste product excretion via nutrient control: Possible strategies for maximizing product and cell yields on serum in cultures of mammalian cells. Biotechnol Bioeng 28(9): 1376-1389.
24. Häggström L. 2000. Cell metabolism, animal. In: Stier R, editor. Encyclopedia of cell technology. New York: Wiley & Sons, p 392-411.
25. Hassell T, Butler M. 1990. Adaptation to non-ammoniagenic medium and selective substrate feeding lead to enhanced yields in animal cell cultures. J Cell Sci 96(Pt 3): 501-508.
26. Irani N, Wirth M, van den Heuvel J, Wagner R. 1999. Improvement of the primary metabolism of cell cultures by introducing a new cytoplasmic pyruvate carboxylase reaction. Biotechnol Bioeng 66(4): 238-246.
27. 6-tagged glycerokinase from Pichia farinosa for enzymatic cycling assays in mammalian cells. J Biotechnol 150(3): 396-403.
28. Janke R, Genzel Y, Wahl A, Reichl U. 2010b. Measurement of key metabolic enzyme activities in mammalian cells using rapid and sensitive microplate-based assays. Biotechnol Bioeng 107(3): 566-581.
29. Kvamme E, Roberg B, Torgner IA. 2000. Phosphate-activated glutaminase and mitochondrial glutamine transport in the brain. Neurochem Res 25(9-10): 1407-1419.
30. Leveille GA, Hanson RW. 1966. Adaptive changes in enzyme activity and metabolic pathways in adipose tissue from meal-fed rats. J Lipid Res 7(1): 46-55.
31. Ljunggren J, Häggström L. 1994. Catabolic control of hybridoma cells by glucose and glutamine limited fed-batch cultures. Biotechnol Bioeng 44(7): 808-818.
32. McCarthy DJ, Smyth GK. 2009. Testing significance relative to a fold-change threshold is a TREAT. Bioinformatics 25(6): 765-771.
33. McDermott RH, Butler M. 1993. Uptake of glutamate, not glutamine synthetase, regulates adaptation of mammalian cells to glutamine-free medium. J Cell Sci 104(Pt 1): 51-58.
34. Merten OW, Kierulff JV, Castignolles N, Perrin P. 1994. Evaluation of the new serum free medium (MDSS2) for the production of different biologicals: Use of various cell lines. Cytotechnology 14(1): 47-59.
35. 13C isotopic tracers for metabolic flux analysis in mammalian cells. J Biotechnol 144(3): 167-174.
36. Molloy MP, Brzezinski EE, Hang JQ, McDowell MT, VanBogelen RA. 2003. Overcoming technical variation and biological variation in quantitative proteomics. Proteomics 3(10): 1912-1919.
37. Neermann J, Wagner R. 1996. Comparative analysis of glucose and glutamine metabolism in transformed mammalian cell lines, insect and primary liver cells. J Cell Physiol 166(1): 152-169.
38. Newsholme EA, Crabtree B. 1986. Maximum catalytic activity of some key enzymes in provision of physiologically useful information about metabolic fluxes. J Exp Zool 239(2): 159-167.
39. Newsholme P, Lima MMR, Porcopio J, Pithon-Curi TC, Doi SQ, Bazotte RB, Curi R. 2003. Glutamine and glutamate as vital metabolites. Braz J Med Biol Res 36(2): 153-163.
40. Ozturk SS, Riley MR, Palsson BO. 1992. Effects of ammonia and lactate on hybridoma growth, metabolism, and antibody production. Biotechnol Bioeng 39(4): 418-431.
41. Reitzer LJ, Wice BM, Kennell D. 1979. Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. J Biol Chem 254(8): 2669-2676.
42. Ritter JB, Genzel Y, Reichl U. 2008. Simultaneous extraction of several metabolites of energy metabolism and related substances in mammalian cells: Optimization using experimental design. Anal Biochem 373(2): 349-369.
43. Rossell S, Solem C, Jensen PR, Heijnen JJ. 2011. Towards a quantitative prediction of the fluxome from the proteome. Metab Eng 13(3): 253-262. DOI: 10.1016/j.ymben.2011.01.010.
44. Sanders PG, Wilson RH. 1984. Amplification and cloning of the Chinese hamster glutamine synthetase gene. EMBO J 3(1): 65-71.
45. Sanfeliu A, Stephanopoulos G. 1999. Effect of glutamine limitation on the death of attached Chinese hamster ovary cells. Biotechnol Bioeng 64(1): 46-53.
46. Segner H, Verreth J. 1995. Metabolic enzyme activities in larvae of the African catfish, Clarias gariepinus: Changes in relation to age and nutrition. Fish Physiol Biochem 14(5): 385-398.
47. Sevdalian DA, Ozand PT, Zielke HR. 1980. Increase in glutaminase activity during the growth cycle of cultured human diploid fibroblasts. Enzyme 25(2): 142-144.
48. Sidorenko Y, Wahl A, Dauner M, Genzel Y, Reichl U. 2008. Comparison of metabolic flux distributions for MDCK cell growth in glutamine- and pyruvate-containing media. Biotechnol Prog 24(2): 311-320.
49. Stanton RC, Seifter JL. 1988. Epidermal growth factor rapidly activates the hexose monophosphate shunt in kidney cells. Am J Physiol 254(2): C267-C271.
50. Stanton RC, Seifter JL, Boxer DC, Zimmerman E, Cantley LC. 1991. Rapid release of bound glucose-6-phosphate dehydrogenase by growth factors. Correlation with increased enzymatic activity. J Biol Chem 266(19): 12442-12448.
51. Stitt M, Sulpice R, Keurentjes J. 2010. Metabolic networks: How to identify key components in the regulation of metabolism and growth. Plant Physiol 152(2): 428-444.
52. 15N n.m.r. study of nitrogen metabolism in cultured mammalian cells. Biochem J 291: 485-492.
53. Stryer L. 1995. Biochemistry. New York: W.H. Freeman. xxxiv, 1064 p.
54. Suarez RK, Staples JF, Lighton JRB, West TG. 1997. Relationships between enzymatic flux capacities and metabolic flux rates: Nonequilibrium reactions in muscle glycolysis. Proc Natl Acad Sci USA 94(13): 7065-7069.
55. Vriezen N, van Dijken JP. 1998. Fluxes and enzyme activities in central metabolism of myeloma cells grown in chemostat culture. Biotechnol Bioeng 59(1): 28-39.
56. Wahl A, Sidorenko Y, Dauner M, Genzel Y, Reichl U. 2008. Metabolic flux model for an anchorage-dependent MDCK cell line: Characteristic growth phases and minimum substrate consumption flux distribution. Biotechnol Bioeng 101(1): 135-152.
57. Yallop CA, Norby PL, Jensen R, Reinbach H, Svendsen I. 2003. Characterisation of G418-induced metabolic load in recombinant CHO and BHK cells: Effect on the activity and expression of central metabolic enzymes. Cytotechnology 42(2): 87-99.
58. Zielke HR, Zielke CL, Ozand PT. 1984. Glutamine: A major energy source for cultured mammalian cells. Fed Proc 43(1): 121-125.