Mapping the yeast host cell response to recombinant membrane protein production: Relieving the biological bottlenecks

Biotechnology Journal

Volumn 6, Issue 6, 2011, Pages 707-714

  Ashe, Mark P ^a   Bill, Roslyn M ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b ASTON UNIVERSITY   (United Kingdom)

Author keywords

Membrane proteins; Protein folding; Stress; Translation; Yeast

Indexed keywords

ACTIVE AREA; CELLULAR PROCESS; EXPERIMENTAL OBSERVATION; GENETIC ANALYSIS; HIGH YIELD; HIGHER YIELD; HOST CELLS; MEMBRANE PROTEINS; NATIVE MEMBRANES; PRESCRIPTION DRUGS; PROTEIN PRODUCTION; PROTEIN SYNTHESIS; RATIONAL OPTIMIZATION; RECOMBINANT HOSTS; TRANSCRIPTOMES; TRANSLATION; TRIAL AND ERROR; WASTE PRODUCTS; YEAST CELL;

BIOLOGICAL MEMBRANES; BIOSYNTHESIS; GENES; MEMBRANES; PROTEIN FOLDING; YEAST;

PROTEINS;

MEMBRANE PROTEIN; RECOMBINANT PROTEIN; TRANSCRIPTOME;

CELL GROWTH; FUNGAL CELL; FUNGAL GENE; FUNGAL STRAIN; GENE IDENTIFICATION; HOST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REVIEW; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; UNFOLDED PROTEIN RESPONSE; YEAST;

GENE EXPRESSION PROFILING; GTP-BINDING PROTEINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; YEASTS;

EID: 79957834961     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201000333     Document Type: Review

References (49)

1. Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W. et al., The sequence of the human genome. Science 2001, 291, 1304-1351.
2. Graf, A., Dragosits, M., Gasser, B., Mattanovich, D., Yeast systems biotechnology for the production of heterologous proteins. FEMS Yeast Res. 2009, 9, 335-348.
3. Park, J. H., Lee, S. Y., Kim, T. Y., Kim, H. U., Application of systems biology for bioprocess development. Trends Biotechnol. 2008, 26, 404-412.
4. Bonander, N., Hedfalk, K., Larsson, C., Mostad, P. et al., Design of improved membrane protein production experiments: Quantitation of the host response. Protein Sci. 2005, 14, 1729-1740.
5. Bonander, N., Darby, R. A., Grgic, L., Bora, N. et al., Altering the ribosomal subunit ratio in yeast maximizes recombinant protein yield. Microb. Cell Fact. 2009, 8, 10.
6. Islam, R. S., Tisi, D., Levy, M. S., Lye, G. J., Framework for the rapid optimization of soluble protein expression in Escherichia coli combining microscale experiments and statistical experimental design. Biotechnol. Prog. 2007, 23, 785-793.
7. Bibi, E., Early targeting events during membrane protein biogenesis in Escherichia coli. Biochim. Biophys. Acta 2011, doi:10.1016/j.bbamem.2010.07.025.
8. Wickner, W., Schekman, R., Protein translocation across biological membranes. Science 2005, 310, 1452-1456.
9. Petaja-Repo, U. E., Hogue, M., Laperriere, A., Walker, P., Bouvier, M., Export from the endoplasmic reticulum represents the limiting step in the maturation and cell surface expression of the human delta opioid receptor. J. Biol. Chem. 2000, 275, 13727-13736.
10. Ward, C. L., Kopito, R. R., Intracellular turnover of cystic fibrosis transmembrane conductance regulator. Inefficient processing and rapid degradation of wild-type and mutant proteins. J. Biol. Chem. 1994, 269, 25710-25718.
11. Tate, C. G., Whiteley, E., Betenbaugh, M. J., Molecular chaperones stimulate the functional expression of the cocaine-sensitive serotonin transporter. J. Biol. Chem. 1999, 274, 17551-17558.
12. Wagner, S., Baars, L., Ytterberg, A. J., Klussmeier, A. et al., Consequences of membrane protein overexpression in Escherichia coli. Mol. Cell Proteomics 2007, 6, 1527-1550.
13. Kunji, E. R., Slotboom, D. J., Poolman, B., Lactococcus lactis as host for overproduction of functional membrane proteins. Biochim. Biophys. Acta 2003, 1610, 97-108.
14. Surade, S., Klein, M., Stolt-Bergner, P. C., Muenke, C. et al., Comparative analysis and "expression space" coverage of the production of prokaryotic membrane proteins for structural genomics. Protein Sci. 2006, 15, 2178-2189.
15. Linares, D. M., Geertsma, E. R., Poolman, B., Evolved Lactococcus lactis strains for enhanced expression of recombinant membrane proteins. J. Mol. Biol. 2010, 401, 45-55.
16. Sevastsyanovicha, Y., Alfasia, S., Cole, J., Recombinant protein production: A comparative view on host physiology New Biotechnol. 2009, 25, 175-180.
17. Wu, P. Y. J., Ruhlmann, C., Winston, F., Schultz, P., Molecular architecture of the S. cerevisiae SAGA complex. Mol. Cell 2004, 15, 199-208.
18. Hoffmann, F., Rinas, U., On-line estimation of the metabolic burden resulting from the synthesis of plasmid-encoded and heat-shock proteins by monitoring respiratory energy generation. Biotechnol. Bioeng. 2001, 76, 333-340.
19. Barford, J. P., A general model for aerobic yeast growth: Batch growth. Biotechnol. Bioeng. 1990, 35, 907-920.
20. Kidane, A., Guan, Y., Evans, P., Kaderbhai, M., Kemp, R., Comparison of heat flux in wild-type and genetically-engineered chinese hamster ovary cells. J. Thermal Anal. 1997, 49, 771-783.
21. Gill, N. K., Appleton, M., Lye, G. J., Thermal profiling for parallel on-line monitoring of biomass growth in miniature stirred bioreactors. Biotechnol. Lett. 2008, 30, 1571-1575.
22. Wagner, S., Klepsch, M. M., Schlegel, S., Appel, A. et al., Tuning Escherichia coli for membrane protein overexpression. Proc. Natl. Acad. Sci. USA 2008, 105, 14371-14376.
23. Singh, S., Gras, A., Fiez-Vandal, C., Ruprecht, J. et al., Large-scale functional expression of WT and truncated human adenosine A2A receptor in Pichia pastoris bioreactor cultures. Microb. Cell Fact. 2008, 7, 28.
24. Mattanovich, D., Gasser, B., Hohenblum, H., Sauer, M., Stress in recombinant protein producing yeasts. J. Biotechnol. 2004, 113, 121-135.
25. Bonander, N., Ferndahl, C., Mostad, P., Wilks, M. D. et al., Transcriptome analysis of a respiratory Saccharomyces cerevisiae strain suggests the expression of its phenotype is glucose insensitive and predominantly controlled by Hap4, Cat8 and Mig1. BMC Genomics 2008, 9, 365.
26. Ferndahl, C., Bonander, N., Logez, C., Wagner, R. et al., Increasing cell biomass in Saccharomyces cerevisiae increases recombinant protein yield: The use of a respiratory strain as a microbial cell factory. Microb. Cell Fact. 2010, 9, 47.
27. O'Malley, M. A., Mancini, J. D., Young, C. L., McCusker, E. C. et al., Progress toward heterologous expression of active G-protein-coupled receptors in Saccharomyces cerevisiae: Linking cellular stress response with translocation and trafficking. Protein Sci. 2009, 18, 2356-2370.
28. Ohya, T., Hayashi, T., Kiyama, E., Nishii, H. et al., Improved production of recombinant human antithrombin III in Chinese hamster ovary cells by ATF4 overexpression. Biotechnol. Bioeng. 2008, 100, 317-324.
29. Omasa, T., Takami, T., Ohya, T., Kiyama, E. et al., Overexpression of GADD34 enhances production of recombinant human antithrombin III in Chinese hamster ovary cells. J. Biosci. Bioeng. 2008, 106, 568-573.
30. Valkonen, M., Penttila, M., Saloheimo, M., Effects of inactivation and constitutive expression of the unfolded- protein response pathway on protein production in the yeast Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2003, 69, 2065-2072.
31. Xu, P., Raden, D., Doyle, F. J. 3rd, Robinson, A. S., Analysis of unfolded protein response during single-chain antibody expression in Saccaromyces cerevisiae reveals different roles for BiP and PDI in folding. Metab. Eng. 2005, 7, 269-279.
32. Mori, K., Signalling pathways in the unfolded protein response: Development from yeast to mammals. J. Biochem. 2009, 146, 743-750.
33. Griffith, D. A., Delipala, C., Leadsham, J., Jarvis, S. M., Oesterhelt, D., A novel yeast expression system for the overproduction of quality-controlled membrane proteins. FEBS Lett. 2003, 553, 45-50.
34. Guerfal, M., Ryckaert, S., Jacobs, P. P., Ameloot, P. et al., The HAC1 gene from Pichia pastoris: Characterization and effect of its overexpression on the production of secreted, surface displayed and membrane proteins. Microb. Cell Fact. 2010, 9, 49.
35. Patil, C., Walter, P., Intracellular signaling from the endoplasmic reticulum to the nucleus: The unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 2001, 13, 349-355.
36. Wentz, A. E., Shusta, E. V., Enhanced secretion of heterologous proteins from yeast by overexpression of ribosomal subunit RPP0. Biotechnol. Prog. 2008, 24, 748-756.
37. Steffensen, L., Pedersen, P. A., Heterologous expression of membrane and soluble proteins derepresses GCN4 mRNA translation in the yeast Saccharomyces cerevisiae. Eukaryotic Cell 2006, 5, 248-261.
38. Pavitt, G. D., eIF2B, a mediator of general and gene-specific translational control. Biochem. Soc. Trans. 2005, 33, 1487-1492.
39. Bourbon, H. M., Aguilera, A., Ansari, A. Z., Asturias, F. J. et al., A unified nomenclature for protein subunits of Mediator complexes linking transcriptional regulators to RNA polymerase II. Mol. Cell 2004, 14, 553-557.
40. Gilbert, W. V., Zhou, K., Butler, T. K., Doudna, J. A., Cap-independent translation is required for starvation-induced differentiation in yeast. Science 2007, 317, 1224-1227.
41. Krynetski, E. Y., Drutsa, V. L., Kovaleva, I. E., Luzikov, V. N., High yield expression of functionally active human liver CYP2D6 in yeast cells. Pharmacogenetics 1995, 5, 103-109.
42. Wegierski, T., Billy, E., Nasr, F., Filipowicz, W., Bms1p, a G-domain-containing protein, associates with Rcl1p and is required for 18S rRNA biogenesis in yeast. RNA 2001, 7, 1254-1267.
43. Gelperin, D., Horton, L., Beckman, J., Hensold, J., Lemmon, S. K., Bms1p, a novel GTP-binding protein, and the related Tsr1p are required for distinct steps of 40S ribosome biogenesis in yeast. RNA 2001, 7, 1268-1283.
44. Karbstein, K., Doudna, J. A., GTP-dependent formation of a ribonucleoprotein subcomplex required for ribosome biogenesis. J. Mol. Biol. 2006, 356, 432-443.
45. Holmes, L. E., Campbell, S. G., De Long, S. K., Sachs, A. B., Ashe, M. P., Loss of translational control in yeast compromised for the major mRNA decay pathway. Mol. Cell Biol. 2004, 24, 2998-3010.
46. Volarevic, S., Stewart, M. J., Ledermann, B., Zilberman, F. et al., Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science 2000, 288, 2045-2047.
47. De Schutter, K., Lin, Y. C., Tiels, P., Van Hecke, A. et al., Genome sequence of the recombinant protein production host Pichia pastoris. Nat. Biotechnol. 2009, 27, 561-566.
48. Gasser, B., Sauer, M., Maurer, M., Stadlmayr, G., Mattanovich, D., Transcriptomics-based identification of novel factors enhancing heterologous protein secretion in yeasts. Appl. Environ. Microbiol. 2007, 73, 6499-6507.
49. Bonander, N., Bill, R. M., Relieving the first bottleneck in the drug discovery pipeline: Using array technologies to rationalize membrane protein production. Expert Rev. Proteomics 2009, 6, 501-505.