Rescue of immunoglobulins from insolubility is facilitated by PDI in the baculovirus expression system

Protein Expression and Purification

Volumn 7, Issue 3, 1996, Pages 281-288

  Hsu, Tsu An ^a   Watson, Sarah ^a   Eiden, Joseph J ^b,c   Betenbaugh, Michael J ^a  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; CAPRA HIRCUS; CYPOVIRUS; INSECTA; TRICHOPLUSIA NI; UNIDENTIFIED BACULOVIRUS;

EID: 0030151987     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1006/prep.1996.0040     Document Type: Article

References (49)

1. 1. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains. Science 181, 223-230.
2. 2. Gething, M. J., and Sambrook, J. (1992) Protein folding in the cell. Nature 355, 33-45.
3. 3. Freedman, R. B., Hirst, T. R., and Tuite, M. F. (1994) Protein disulphide Isomerase: Building bridges in protein folding. Trends Biochem. Sci. 19, 331-336.
4. 4. Wittrup, K. D. (1995) Disulfide bond formation and eukaryotic secretory productivity. Curr. Opin. Biotechnol. 6, 203-208.
5. 5. Bulleid, N. J., and Freedman, R. B. (1988) Defective co-translational formation of disulfide bonds in protein disulfide-isomerase-deficient microsomes. Nature 335, 649-651.
6. 6. Lamantia, M.-L., and Lennarz, W. J. (1993) The essential function of yeast protein disulfide isomerase does not reside in its isomerase activity. Cell 74, 899-908.
7. 7. Vuori, K., Pihlajaniemi, T., Marttila, M., and Kivirikko, K. I. (1992) Characterization of the human prolyl 4-hydroxylase tetramer and its multifunctional protein disulfide-isomerase subunit synthesized in a baculovirus expression system. Proc. Natl. Acad. Sci. USA 89, 7467-7470.
8. 8. Wetterau, J. R., Combs, K. A., McLean, L. R., Spinner, S. N., and Aggerbeck, L. P. (1991) Protein disulfide isomerase appears necessary to maintain the catalytically active structure of the microsomal triglyceride transfer protein. Biochemistry 30, 9728-9735.
9. 9. Noiva, R., and Lennarz, W. J. (1992) Protein disulfide isomerase. J. Biol. Chem. 267, 3553-3556.
10. 10. Puig, A., and Gilbert, H. F. (1994) Protein disulfide isomerase exhibits chaperone and anti-chaperone activity in the oxidative refolding of lysozyme. J. Biol. Chem. 269, 7764-7771.
11. 11. Freedman, R. B., Bulleid, N. J., Hawkins, H. C., and Paver, J. L. (1988) Role of protein disulfide-isomerase in the expression of native proteins. Biochem. Soc. Symp. 55, 167-192.
12. 12. Roth, R. A., and Koshland, M. E. (1981) Role of disulfide interchange enzyme in immunoglobulin synthesis. Biochemistry 20, 6594-6599.
13. 13. Roth, R. A., and Pierce, S. B. (1987) In vivo cross-linking of protein disulfide isomerase to immunoglobulins. Biochemistry 26, 4179-4182.
14. 14. Corte, E. D., and Parkhouse, R. M. E. (1973) Biosynthesis of immunoglobulin A (IgA) and immunoglobulin M (IgM). Biochem. J. 136, 597-606.
15. 15. Lilie, H., McLaughlin, S., Freedman, R., and Buchner, J. (1994) Influence of protein disulfide isomerase (PDI) on antibody folding in vitro. J. Biol. Chem. 269, 14290-14296.
16. 16. Hurtley, S. M., Bole, D. G., Hoover-Litty, Helenius, A., and Copeland, C. S. (1989) Interaction of misfolded influenza virus hemmagglutinin with binding protein (BiP). J. Cell Biol. 108, 2117-2126.
17. 17. Marquardt, T., and Helenius, A. (1992) Misfolding and aggregation of newly synthesized proteins in the endoplasmic reticulum. J. Cell Biol. 117, 505-513.
18. 18. Kim, P. S., and Arvan, P. (1991) Folding and assembly of newly synthesized thyroglobulin occurs in a pre-Golgi compartment. J. Biol. Chem. 266, 12412-12418.
19. 19. Braakman, I., Helenius, J., and Helenius, A. (1993) Role of ATP and disulfide bonds during protein folding in the endoplasmic reticulum. Nature 356, 260-262.
20. 20. de Silva, A., Braakman, I., and Helenius, A. (1993) Posttranslational folding of vesicular stomatitis virus G protein in the ER: Involvement of noncovalent and covalent complexes. J. Cell Biol. 120, 647-655.
21. 21. Rothman, J. E. (1989) Polypeptide chain binding proteins: Catalysts of protein folding and related processes in cells. Cell 59, 591-601.
22. 22. Mazzarella, R. A., Srinivasan, M., Haugejorden, S. M., and Green, M. (1990) ERp72, an abundant luminal endoplasmic reticulum protein, contains three copies of the active site sequence of protein disulfide isomerase. J. Biol. Chem. 265, 1094-1101.
23. 23. zu Putlitz, J., Kubasek, W. L., Duchene, M., Marget, M., von Specht, B.-U., and H. Domdey (1990) Antibody production in baculovirus-infected insect cells. Biotechnology 8, 651-654.
24. 24. Summers, M. D., and Smith, G. (1987) "A Manual of Methods for Baculovirus Vectors and Insect Cell Culture Procedures," Bulletin No. 1555, Texas Agricultural Experiment Station and Texas A&M University, College Station, TX.
25. 25. Jeang, K. T., Giam, C. Z., Nierenberg, and Khoury, G. (1987) Abundant synthesis of functional HTLV-1 p40x protein in eucaryotic cells by using baculovirus expression vectors. J. Virol. 61, 708-713.
26. 26. Lindsay, D. A., Vonderfecht, S. L., Betenbaugh, M. J., and Eiden, J. J. (1993) Baculovirus expression of gene 6 of the IDIR strain of group B rotavirus (GBR): Coding assignment of the major inner capsid protein. Virology 193, 367-375.
27. 27. Davis, T. R., Munkenbeck, Trotter, K., Granados, R. R., and Wood, H. A. (1992) Baculovirus expression of alkaline phosphatase as a reporter gene for evaluation of production, glycosylation and secretion. Biotechnology 10, 1148-1150.
28. 28. Hsu, T.-A., Eiden, J. J., Bourgarel, P., Meo, T., and Betenbaugh, M. J. (1994) Effects of coexpressing chaperone BiP on functional antibody production in the baculovirus system. Protein Expression Purif. 5, 595-603.
29. 29. Petersen, J. G. L., and Dorrington, K. J. (1974) An in vitro system for studying the kinetics of interchain disulfide bond formation in immunoglobulin G. J. Biol. Chem. 249, 5633-5641.
30. 30. Mullis, K. B., and Faloona, F. A. (1987) Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 155, 335.
31. 31. Haseman, C. A., and Capra, J. D. (1990) High-level production of a functional immunoglobulin heterodimer in a baculovirus expression system. Proc. Natl. Acad. Sci. USA 87, 3942-3946.
32. 32. Jarvis, D. L., and Summers, M. D. (1989) Glycosylation and secretion of human tissue plasminogen activator in recombinant baculovirus-infected insect cells. Mol. Cell. Biol. 9, 214-223.
33. 33. Hickman, S., and Kornfeld, S. (1978) Effect of tunicamycin on IgM, IgA, and IgG secretion by mouse plasmacytoma cells. J. Immunol. 121, 990-996.
34. 34. Percy, M. E., Baumal, R., Dorrington, K. J., and Percy, J. R. (1976) Covalent assembly of mouse immunoglobulin G sub-classes in vitro: Application of a theoretical model for interchain disulfide bond formation. Can. J. Biochem. 54, 675-687.
35. 35. Kishida, F., Azuma, T., and Hamaguchi, K. (1976) Formation of interchain disulfide bonds in Bence Jones protein and immunoglobulins. J. Biochem. 79, 91-105.
36. 36. Valetti, C., Grossi, C. E., Milstein, C., and Sitia, R. (1991) Russell bodies: A general response of secretory cells to synthesis of a mutant immunoglobulin which can neither exit from, nor be degraded in, the endoplasmic reticulum. J. Cell Biol. 115, 983-994.
37. 37. Robinson, A. S., Himes, V., and Wittrup, K. D. (1994) Protein disulfide isomerase overexpression increases secretion of foreign protein in Saccharomyces cerevisiae. Biotechnology 12, 381-385.
38. 38. Schultz, L., Markus, H., Hoffmann, K., Montgomery, D., Dunwiddie, C., Kniskern, P., Freedman, R., Ellis, R., and Tuite, M. (1994) Using molecular-genetics to improve the production of recombinant proteins by the yeast Saccharomyces cerevisiae. Ann. NY Acad. Sci. 721, 148-157.
39. 39. Noiva, R. (1995) Enzymatic catalysis of disulfide formation. Protein Expression Purif. 5, 1-13.
40. 40. Hwang, C., Sinskey, A., and Lodish, H. F. (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257, 1496-1502.
41. 41. Lyles, M. M., and Gilbert, H. F. (1991) Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: Dependence of the rate on the composition of the redox buffer. Biochemistry 30, 613-619.
42. 42. Lundstrom, J., and Holmgren, A. (1992) Protein disulfide-isomerase is a substrate for thioredoxin reductase and has thioredoxin-like activity. J. Biol. Chem. 265, 9114-9120.
43. 43. Dorner, A. J., Wasley, L. C., Raney, P., Haugejorden, S., Green, M., and Dauffman, R. J. (1990) The stress response in Chinese hamster ovary cells. J. Biol. Chem. 265, 22029-22034.
44. 44. Lodish, H. F., and Kong, N. (1993) The secretory pathway is normal in dithiothreitol-treated cells, but disulfide-bonded proteins are reduced and reversibly retained in the endoplasmic reticulum. J. Biol. Chem. 268, 20598-20605.
45. 45. Weissman, J. S., and Kim, P. S. (1993) Efficient catalysis of disulfide bond rearrangements by protein disulfide isomerase. Nature 365, 185-188.
46. 46. Gilbert, H. F. (1994) Protein chaperones and protein folding. Curr. Opin. Biotechnol. 5, 534-539.
47. 47. Gai, H., Wang, C.-C., and Tsou, C.-L. (1994) Chaperone-like activity of protein disulfide isomerase in the refolding of a protein with no disulfide bonds. J. Biol. Chem. 269, 24550-24552.
48. 48. Milstein, C., Brownlee, G. G., Harrison, T. M., and Mathews, M. B. (1972) A possible precursor of immunoglobulin light chains. Nature New Biol. 239, 117-120.
49. 49. Chessler, S. D., and Byers, P. H. (1992) Defective folding and stable association with protein disulfide isomerase/prolyl hydroxylase of type-I procollagen with a deletion in the pro-alpha-2(I) chain that preserves the Gly-X-Y repeat pattern. J. Biol. Chem. 267, 7751-7757.