Understanding translational control mechanisms of the mTOR pathway in CHO cells by polysome profiling

New Biotechnology

Volumn 31, Issue 5, 2014, Pages 514-523

  Courtes, Franck C ^a,b   Vardy, Leah ^c   Wong, Niki S C ^d   Bardor, Muriel ^a   Yap, Miranda G S ^a,b   Lee, Dong Yup ^a,b  

^a AGENCY FOR SCIENCE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^d ABBVIE INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; ANTIBODIES; BATCH CELL CULTURE; CELL CULTURE; CELLS; CYTOLOGY; MAMMALS; MOBILE SECURITY; MONOCLONAL ANTIBODIES; NUTRIENTS;

CELLULAR GROWTH RATE; HEAVY AND LIGHT CHAINS; MAMMALIAN TARGET OF RAPAMYCIN (MTOR); MOLECULAR MECHANISM; MONOCLONAL ANTIBODIES (MAB); POLYSOME PROFILING; RAPAMYCIN TREATMENT; TRANSLATION ACTIVITY;

TRANSLATION (LANGUAGES);

GLUCOSE; GLUTAMINE; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MONOCLONAL ANTIBODY; RAPAMYCIN; RECOMBINANT ANTIBODY; IMMUNOSUPPRESSIVE AGENT; RECOMBINANT PROTEIN; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIUM CULTURE; CELL ACTIVITY; CELL CULTURE; CELL FRACTIONATION; CELL GROWTH; CHO CELL LINE; CLINICAL EVALUATION; CONTROLLED STUDY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME MECHANISM; FED BATCH CULTURE; FEEDING; FEMALE; FOOD INTAKE; GROWTH CURVE; HEAVY CHAIN; HUMAN; HUMAN CELL; LIGHT CHAIN; MOLECULAR BIOLOGY; NONHUMAN; NUTRIENT AVAILABILITY; NUTRIENT LIMITATION; NUTRITIONAL SUPPORT; POLYSOME; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; ANIMAL; BIOSYNTHESIS; CRICETULUS; DRUG EFFECTS; HAMSTER; METABOLISM; PROTEIN SYNTHESIS;

EUKARYOTA; MAMMALIA;

ANIMALS; ANTIBODIES, MONOCLONAL; CHO CELLS; CRICETINAE; CRICETULUS; IMMUNOSUPPRESSIVE AGENTS; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RECOMBINANT PROTEINS; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 84925158681     PISSN: 18716784     EISSN: 18764347     Source Type: Journal    
DOI: 10.1016/j.nbt.2013.10.003     Document Type: Article

References (47)

1. Buttgereit F., Brand M.D. A hierarchy of ATP-consuming processes in mammalian cells. Biochem J 1995, 312(Pt 1):163-167.
2. Dethlefsen L., Schmidt T.M. Performance of the translational apparatus varies with the ecological strategies of bacteria. J Bacteriol 2007, 189:3237-3245.
3. Arava Y., Boas F.E., Brown P.O., Herschlag D. Dissecting eukaryotic translation and its control by ribosome density mapping. Nucleic Acids Res 2005, 33:2421-2432.
4. Preiss T., Baron-Benhamou J., Ansorge W., Hentze M.W. Homodirectional changes in transcriptome composition and mRNA translation induced by rapamycin and heat shock. Nat Struct Biol 2003, 10:1039-1047.
5. Sampath P., Pritchard D.K., Pabon L., Reinecke H., Schwartz S.M., Morris D.R., et al. A hierarchical network controls protein translation during murine embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2008, 2:448-460.
6. Thomas J.D., Johannes G.J. Identification of mRNAs that continue to associate with polysomes during hypoxia. RNA 2007, 13:1116-1131.
7. Uesono Y., Toh E.A. Transient inhibition of translation initiation by osmotic stress. J Biol Chem 2002, 277:13848-13855.
8. Van Ryk D.I., Lee Y., Nazar R.N. Unbalanced ribosome assembly in Saccharomyces cerevisiae expressing mutant 5 S rRNAs. J Biol Chem 1992, 267:16177-16181.
9. Valasek L., Nielsen K.H., Hinnebusch A.G. Direct eIF2-eIF3 contact in the multifactor complex is important for translation initiation in vivo. EMBO J 2002, 21:5886-5898.
10. Seggerson K., Tang L., Moss E.G. Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev Biol 2002, 243:215-225.
11. Masek T., Valasek L., Pospisek M. Polysome analysis and RNA purification from sucrose gradients. Methods Mol Biol 2011, 703:293-309.
12. Courtes F.C., Lin J., Lim H.L., Ng S.W., Wong N.S.C., Koh G., et al. Translatome analysis of CHO cells to identify key growth genes. J Biotechnol 2013, 167:215-224.
13. Gibbons J.J., Abraham R.T., Yu K. Mammalian target of rapamycin: discovery of rapamycin reveals a signaling pathway important for normal and cancer cell growth. Semin Oncol 2009, 36(Suppl. 3):S3-S17.
14. Foster K.G., Fingar D.C. Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony. J Biol Chem 2010, 285:14071-14077.
15. Ma X.M., Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 2009, 10:307-318.
16. Li Y., Corradetti M.N., Inoki K., Guan K.L. TSC2: filling the GAP in the mTOR signaling pathway. Trends Biochem Sci 2004, 29:32-38.
17. Hay N., Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004, 18:1926-1945.
18. Campbell L.E., Wang X., Proud C.G. Nutrients differentially regulate multiple translation factors and their control by insulin. Biochem J 1999, 344(Pt 2):433-441.
19. Dennis P.B., Jaeschke A., Saitoh M., Fowler B., Kozma S.C., Thomas G. Mammalian TOR: a homeostatic ATP sensor. Science 2001, 294:1102-1105.
20. Brugarolas J., Lei K., Hurley R.L., Manning B.D., Reiling J.H., Hafen E., et al. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev 2004, 18:2893-2904.
21. Reiling J.H., Sabatini D.M. Stress and mTORture signaling. Oncogene 2006, 25:6373-6383.
22. Barbet N.C., Schneider U., Helliwell S.B., Stansfield I., Tuite M.F., Hall M.N. TOR controls translation initiation and early G1 progression in yeast. Mol Biol Cell 1996, 7:25-42.
23. Zhou L., Goldsmith A.M., Bentley J.K., Jia Y., Rodriguez M.L., Abe M.K., et al. 4E-binding protein phosphorylation and eukaryotic initiation factor-4E release are required for airway smooth muscle hypertrophy. Am J Resp Cell Mol Biol 2005, 33:195-202.
24. Dreesen I.A., Fussenegger M. Ectopic expression of human mTOR increases viability, robustness, cell size, proliferation, and antibody production of Chinese hamster ovary cells. Biotechnol Bioeng 2011, 108:853-866.
25. Lee J.S., Lee G.M. Rapamycin treatment inhibits CHO cell death in a serum-free suspension culture by autophagy induction. Biotechnol Bioeng 2012, 109:3093-3102.
26. Hara K., Yonezawa K., Weng Q.P., Kozlowski M.T., Belham C., Avruch J. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J Biol Chem 1998, 273:14484-14494.
27. Chong W.P., Sim L.C., Wong K.T., Yap M.G. Enhanced IFNgamma production in adenosine-treated CHO cells: a mechanistic study. Biotechnol Progr 2009, 25:866-873.
28. Patel J., Wang X., Proud C.G. Glucose exerts a permissive effect on the regulation of the initiation factor 4E binding protein 4E-BP1. Biochem J 2001, 358:497-503.
29. Eldad N., Arava Y. A ribosomal density-mapping procedure to explore ribosome positions along translating mRNAs. Methods Mol Biol 2008, 419:231-242.
30. Chusainow J., Yang Y.S., Yeo J.H., Toh P.C., Asvadi P., Wong N.S., et al. A study of monoclonal antibody-producing CHO cell lines: what makes a stable high producer?. Biotechnol Bioeng 2009, 102:1182-1196.
31. Ikenoue T., Hong S., Inoki K. Monitoring mammalian target of rapamycin (mTOR) activity. Methods Enzymol 2009, 452:165-180.
32. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
33. Choo A.Y., Yoon S.O., Kim S.G., Roux P.P., Blenis J. Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci U S A 2008, 105:17414-17419.
34. Balcarcel R.R., Stephanopoulos G. Rapamycin reduces hybridoma cell death and enhances monoclonal antibody production. Biotechnol Bioeng 2001, 76:1-10.
35. Van Dyke N., Baby J., Van Dyke M.W. Stm1p, a ribosome-associated protein, is important for protein synthesis in Saccharomyces cerevisiae under nutritional stress conditions. J Mol Biol 2006, 358:1023-1031.
36. Wall M., Poortinga G., Hannan K.M., Pearson R.B., Hannan R.D., McArthur G.A. Translational control of c-MYC by rapamycin promotes terminal myeloid differentiation. Blood 2008, 112:2305-2317.
37. Han Y.K., Ha T.K., Lee S.J., Lee J.S., Lee G.M. Autophagy and apoptosis of recombinant Chinese hamster ovary cells during fed-batch culture: effect of nutrient supplementation. Biotechnol Bioeng 2011, 108:2182-2192.
38. Sanfeliu A., Stephanopoulos G. Effect of glutamine limitation on the death of attached Chinese hamster ovary cells. Biotechnol Bioeng 1999, 64:46-53.
39. Gingras A.C., Gygi S.P., Raught B., Polakiewicz R.D., Abraham R.T., Hoekstra M.F., et al. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 1999, 13:1422-1437.
40. Mothe-Satney I., Yang D., Fadden P., Haystead T.A., Lawrence Jr J.C. Multiple mechanisms control phosphorylation of PHAS-I in five (S/T)P sites that govern translational repression. Mol Cell Biol 2000, 20:3558-3567.
41. Sonenberg N., Hinnebusch A.G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009, 136:731-745.
42. Foiani M., Cigan A.M., Paddon C.J., Harashima S., Hinnebusch A.G. GCD2, a translational repressor of the GCN4 gene, has a general function in the initiation of protein synthesis in Saccharomyces cerevisiae. Mol Cell Biol 1991, 11:3203-3216.
43. Underhill M.F., Birch J.R., Smales C.M., Naylor L.H. eIF2alpha phosphorylation, stress perception, and the shutdown of global protein synthesis in cultured CHO cells. Biotechnol Bioeng 2005, 89:805-814.
44. Druz A., Chu C., Majors B., Santuary R., Betenbaugh M., Shiloach J. A novel microRNA mmu-miR-466h affects apoptosis regulation in mammalian cells. Biotechnol Bioeng 2011, 108:1651-1661.
45. Thomas G., Hall M.N. TOR signalling and control of cell growth. Curr Opin Chem Biol 1997, 9:782-787.
46. Inoki K., Li Y., Zhu T., Wu J., Guan K.L. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 2002, 4:648-657.
47. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell 2006, 124:471-484.