eIF2α phosphorylation, stress perception, and the shutdown of global protein synthesis in cultured CHO cells

Biotechnology and Bioengineering

Volumn 89, Issue 7, 2005, Pages 805-814

  Underhill, Michèle F ^a   Birch, John R ^b   Smales, C Mark ^a   Naylor, Louise H ^a  

^a UNIVERSITY OF KENT   (United Kingdom)

^b LONZA AG   (Switzerland)

Author keywords

CHO cells; eIF2 phosphorylation; Fed batch culture; Recombinant protein production

Indexed keywords

BIOSYNTHESIS; CELL CULTURE; CELLS; GROWTH KINETICS; RNA;

APOPTOSIS; CELL DEATH; PHOSPHORYLATION; PROTEIN SYNTHESIS;

PROTEINS;

INITIATION FACTOR 2ALPHA; MESSENGER RNA; PROTEIN; RECOMBINANT PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; INITIATION FACTOR 2; METHIONINE; MONOCLONAL ANTIBODY; SULFUR; UBIQUITIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CHO CELL; FED BATCH CULTURE; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RNA TRANSLATION; SIGNAL TRANSDUCTION; STRESS; UBIQUITINATION; ANIMAL; BIOREACTOR; CRICETULUS; DOWN REGULATION; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; HAMSTER; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; OXIDATIVE STRESS; PHOSPHORYLATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; SECRETION; SILVER STAINING; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL; BIOREACTORS; BLOTTING, WESTERN; CHO CELLS; CRICETINAE; CRICETULUS; DOWN-REGULATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EUKARYOTIC INITIATION FACTOR-2; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; KINETICS; METHIONINE; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; RECOMBINANT PROTEINS; SILVER STAINING; SULFUR RADIOISOTOPES; TISSUE INHIBITOR OF METALLOPROTEINASE-1; UBIQUITIN;

EID: 16444368659     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/bit.20403     Document Type: Article

References (52)

1. Baker KN, Rendall MH, Hills AE, Hoare M, Freedman RB, James DC. 2001. Metabolic control of recombinant protein N-glycan processing in NSO and CHO cells. Biotechnol Bioeng 73:188-202.
2. Baker KN, Rendall MH, Patel A, Boyd P, Hoare M, Freedman RB, James DC. 2002. Rapid monitoring of recombinant protein products: a comparison of current technologies. Trends in Biotechnol 20:149-156.
3. Benedetti C, Fabbri M, Sitia R, Cabibbo A. 2000. Aspects of gene regulation during the UPR in human cells. Biochem Biophys Res Com 278:530-536.
4. Berlanga JJ, Santoyo J, de Haro C. 1999. Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2α kinase. Eur J Biochem 265:754-762.
5. Brostrom MA, Lin XJ, Cade C, Gmitter D, Brostrom CO. 1989. Loss of a calcium requirement for protein synthesis in pituitary cells following thermal or chemical stress. J Biol Chem 264:1638-1643.
6. Brostrom CO, Brostrom MA. 1998. Regulation of translational initiation during cellular responses to stress. Prog Nucl Acid Res Mol Biol 58:79-125.
7. Burns KB, Duggan B, Atkinson EA, Famulski KS, Nemer M, Bleackley RC, Michalak M. 1994. Modulation of gene expression by calreticulin binding to the glucocorticoid receptor. Nature 367:476-477.
8. Chen J-J. 2000. Heme-regulated eIF2α kinase. In: Sonenberg N, Hershey JWB, and Mathews MB., editors. Translational control of gene expression. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 529-546.
9. Cockett MI, Bebbington CR, Yarranton GT. 1990. High level expression of tissue inhibitor of metalloproteinases in Chinese Hamster Ovary cells using glutamine synthetase gene amplification. Bio/Technol 8:662-667.
10. Davis R, Schooley K, Rasmussen B, Thomas J, Reddy P. 2000. Effect of PDI overexpression on recombinant protein secretion in CHO cells. Biotechnol Prog 16:736-743.
11. Downham MR, Farrell WE, Jenkins HA. 1996. Endoplasmic reticulum protein expression in recombinant NS0 myelomas grown in batch culture. Biotechnol Bioeng 51:691-696.
12. Fernandez J, Yaman I, Merrick WC, Koromilas A, Wek RC, Sood R, Hensold J, Hatzoglou M. 2002. Regulation of internal ribosome entry site-mediated translation by eukaryotic initiation factor-2α phosphorylation and translation of a small upstream open reading frame. J Biol Chem 277:2050-2058.
13. Frand AR, Cuozzo JW, Kaiser CA. 2000. Pathways for protein disulphide bond formation. Trends in Cell Biol 10:203-210.
14. Freedman RB. 1984. Native disulphide bond formation in protein biosynthesis: Evidence for the role of protein disulphide isomerase. Trends Biochem Sci 9:438-441.
15. Freedman RB, Hirst TR, Tuite MF. 1994. Protein disulfide isomerase: Building bridges in protein folding. TIBS 19:331-336.
16. Fussenegger M, Schlatter S, Datwyler D, Mazur X, Bailey JE. 1998. Controlled proliferation by multigene metabolic engineering enhances the productivity of Chinese hamster ovary cells. Nature Biotech 16:468-472.
17. Gething MJ, Sambrook J. 1992. Protein folding in the cell. Nature 355:33-45.
18. Harding HP, Zhang Y, Ron D. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum resident kinase. Nature 397:271-274.
19. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. 2000a. PERK is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5:897-904.
20. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. 2000b. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108.
21. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D. 2003. An integrated stress response regulates amino acid metabolism resistance to oxidative stress. Mol Cell 11:619-633.
22. Hartl FU. 1996. Molecular chaperones in cellular protein folding. Nature 381:571-579.
23. Heal R, McGivan J. 1998. Induction of calreticulin expression in response to amino acid deprivation in Chinese hamster ovary cells. Biochem J 329:389-394.
24. Helenius A, Trambetta ES, Hebert DN, Simons JF. 1997. Calnexin, Calreticulin & the folding of glycoproteins. Trends Cell Biol 7:193-200.
25. Hinnebusch AG. 1993. Gene-specific translational control of the yeast GCN4 gene by phosphorylation of eukaryotic initiation factor 2. Mol Microbiol 2:215-223.
26. Hu WS, Aunins JG. 1997. Large-scale mammalian cell culture. Curr Opin Biotechnol 8:148-153.
27. Kaufman RJ. 1999a. Double-stranded RNA-activated protein kinase mediates virus-induced apoptosis: A new role for an old actor. Proc Natl Acad Sci USA 96:11693-11695.
28. Kaufman RJ. 1999b. Stress signaling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls. Genes Dev 13:1211-1233.
29. Kimball SR. 2001. Regulation of translation initiation by amino acids in eukaryotic cells. Prog Subcell Biol 26:155-184.
30. Krishnamoorthy T, Pavitt GD, Zhang F, Dever TE, Hinnebusch AG. 2001. Tight binding of the phosphorylated α subunit of initiation factor 2 (eIF2α) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol Cell Biol 21:5018-5030.
31. Laitusis AL, Brostrom MA, Brostrom CO. 1999. The dynamic role of GRP78/BiP in the coordination of mRNA translation with protein processing. J Biol Chem 274:486-493.
32. Ma Y, Brewer JW, Diehl JA, Hendershot LM. 2002. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J Mol Biol 318:1351-1365.
33. Malandro MS, Kilberg MS. 1996. Molecular biology of mammalian amino acid transporters. Annu Rev Biochem 65:305-336.
34. Mastrangelo AJ, Betenbaugh MJ. 1998. Overcoming apoptosis: New methods for improving protein-expression systems. TIBTECH 16:88-95.
35. Mimnaugh EG, Bonvini P, Neckers L. 1999. The measurement of ubiquitin and ubiquitinated proteins. Electrophoresis 20:418-428.
36. Mori K. 2000. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101:451-454.
37. Murphy TC, Woods NR, Dickson AJ. 2001. Expression of the transcription factor GADD153 is an indicator of apoptosis for recombinant Chinese Hamster Ovary (CHO) Cells. Biotechnol Bioeng 75:621-629.
38. Novoa I, Zhang Y, Zeng H, Jungreis R, Harding HP, Ron D. 2003. Stress-induced gene expression requires programmed recovery from translational repression. EMBO 22:1180-1187.
39. Pain VM. 1994. Translational control during amino acid starvation. Biochimie 76:718-728.
40. Pain VM. 1996. Initiation of protein synthesis in eukaryotic cells. Eur J Biochem 236:747-771.
41. Patil C, Walter P. 2001. Intracellular signaling from the endoplasmic reticulum to the nucleus: The unfolded protein response in yeast and mammals. Curr Opin Cell Biol 13:349-355.
42. Plakidou-Dymock S, McGivan JD. 1994. Calreticulin-A stress protein induced in the renal epithelial cell line NBL-1 by amino acid deprivation. Cell Calcium 16:1-8.
43. Rao RV, Peel A, Logvinova A, Del Rio G, Hermel E, Yokota T, Goldsmith PC, Ellerby LM, Ellerby HM, Bredesen DE. 2002. Coupling endoplasmic reticulum stress to the cell death program: Role of the ER chaperone GRP78. FEBS Lett 514:122-128.
44. Rutkowski DT, Kaufman RJ. 2004. A trip to the ER: Coping with stress. Trends Cell Biol 14:20-28.
45. Sarre TF, Hermann M, Bader M. 1989. Differential effect of hemin-controlled eIF-2 alpha kinases from mouse erythroleukemia cell on protein synthesis. Eur J Biochem 183:137-143.
46. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, Kaufman RJ. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7:1165-1176.
47. Schroder M, Friedl P. 1997. Overexpression of recombinant human antithrombin III in Chinese Hamster Ovary cells results in malformation and decreased secretion of recombinant protein. Biotechnol Bioeng 53:547-559.
48. Shoesmith Berke SJ, Paulson HL. 2003. Protein aggregation and the ubiquitin proteasome pathway: Gaining the upper hand on neurodegeneration. Curr Opin Genet Dev 13:253-261.
49. Sood R, Porter AC, Olsen D, Cavener DR, Wek RC. 2000. A mammalian homologue of GCN2 protein kinase important for translational control by phosphorylation of eukaryotic initiation factor-2α. Genetics 154:787-801.
50. Weissman AM. 2001. Themes and variations on ubiquitylation. Nature Rev Mol Cell Biol 2:169-178.
51. Van W, Frank CL, Korth MJ, Sopher BL, Novoa I, Ron D, Katze MG. 2002. Control of PERK eIF2α kinase activity by the endoplasmic stress-induced molecular chaperone P58IPK. Proc Natl Acad Sci USA 99:15920-15925.
52. Zhou W, Chen C-C, Buckland B, Aunins J. 1997. Fed-batch culture of recombinant NS0 myeloma cells with high monoclonal antibody production. Biotechnol Bioeng 55:783-792.