239
Views
4
CrossRef citations to date
0
Altmetric
Original Articles

Genetic and substrate-level modulation of Bacillus subtilis physiology for enhanced extracellular human interferon gamma production

, ORCID Icon, &

References

  • Bolinger, A. M.; Taeubel, M. A. Recombinant Interferon Gamma for Treatment of Chronic Granulomatous Disease and Other Disorders. Clin. Pharm. 1992, 11(10), 834–850; quiz 892–894.
  • Green, D. S.; Young, H. A.; Valencia, J. C. Current Prospects of Type II Interferon γ Signaling and Autoimmunity. J. Biol. Chem. 2017, 292(34), 13925–13933.
  • Razaghi, A.; Owens, L.; Heimann, K. Review of the Recombinant Human Interferon Gamma as an Immunotherapeutic: Impacts of Production Platforms and Glycosylation. J. Biotechnol. 2016, 240, 48–60. DOI: 10.1016/j.jbiotec.2016.10.022.
  • Khalilzadeh, R.; Shojaosadati, S. A.; Maghsoudi, N.; Mohammadian-Mosaabadi, J.; Mohammadi, M. R.; Bahrami, A.; Maleksabet, N.; Nassiri-Khalilli, M. A.; Ebrahimi, M.; Naderimanesh, H. Process Development for Production of Recombinant Human Interferon-Gamma Expressed in Escherichia coli. J. Ind. Microbiol. Biotechnol. 2004, 31(2), 63–69.
  • Reddy, P. K.; Reddy, S. G.; Narala, V. R.; Majee, S. S.; Konda, S.; Gunwar, S.; Reddy, R. C. Increased Yield of High Purity Recombinant Human Interferon-γ Utilizing Reversed Phase Column Chromatography. Protein Expr. Purif. 2007, 52(1), 123–130.
  • Vaiphei, S. T.; Pandey, G.; Mukherjee, K. J. Kinetic Studies of Recombinant Human Interferon-Gamma Expression in Continuous Cultures of E. coli. J. Ind. Microbiol. Biotechnol. 2009, 36(12), 1453–1458.
  • Babaeipour, V.; Shojaosadati, S. A.; Khalilzadeh, R.; Maghsoudi, N.; Farnoud, A. M. Enhancement of Human γ-Interferon Production in Recombinant E. coli Using Batch Cultivation. Appl. Biochem. Biotechnol. 2010, 160(8), 2366–2376.
  • Medina-Rivero, E.; Balderas-Hernández, V. E.; Ordoñez-Acevedo, L. G.; Paz-Maldonado, L. M. T.; Barba-De la Rosa, A. P.; De León-Rodríguez, A. Modified Penicillin Acylase Signal Peptide Allows the Periplasmic Production of Soluble Human Interferon-γ but not of Soluble Human Interleukin-2 by the Tat Pathway in Escherichia coli. Biotechnol. Lett. 2007, 29(9), 1369–1374.
  • Balderas Hernández, V. E.; Paz Maldonado, L. M. T.; Medina Rivero, E.; Barba de la Rosa, A. P.; Jiménez-Bremont, J. F.; Ordoñez Acevedo, L. G.; De León Rodríguez, A. Periplasmic Expression and Recovery of Human Interferon Gamma in Escherichia coli. Protein. Expr. Purif. 2008, 59(1), 169–174.
  • Wang, D.; Ren, H.; Xu, J.-W.; Sun, P.-D.; Fang, X.-D. Expression, Purification and Characterization of Human Interferon-γ in Pichia pastoris. Mol. Med. Rep. 2014, 9(2), 715–719.
  • Prabhu, A. A.; Veeranki, V. D.; Dsilva, S. J. Improving the Production of Human Interferon Gamma (hIFN-γ) in Pichia pastoris Cell Factory: An Approach of Cell Level. Process Biochem. 2016, 51(6), 709–718.
  • Razaghi, A.; Tan, E.; Lua, L. H. L.; Owens, L.; Karthikeyan, O. P.; Heimann, K. Is Pichia pastoris a Realistic Platform for Industrial Production of Recombinant Human Interferon Gamma? Biologicals 2017, 45, 52–60.
  • Schumann, W. Production of Recombinant Proteins in Bacillus subtilis. In Allen, I., Laskin, S. S., GMG, Eds.; Academic Press, San Diego, 2007; pp 137–189.
  • Ilk, N.; Schumi, C.-T.; Bohle, B.; Egelseer, E. M.; Sleytr, U. B. Expression of an Endotoxin-Free S-Layer/Allergen Fusion Protein in Gram-Positive Bacillus subtilis 1012 for the Potential Application as Vaccines for Immunotherapy of Atopic Allergy. Microb. Cell Factories. 2011, 10(1), 6.
  • Posten, C.; Rinas, U. Control Strategies for High-Cell Density Cultivation of Escherichia coli. In Schügerl, K., Bellgardt, K-H., Eds.; Springer: Berlin, Heidelberg, 2000; pp 374–990.
  • Yeh, C. M.; Yeh, C. K.; Hsu, X. Y.; Luo, Q. M.; Lin, M. Y. Extracellular Expression of a Functional Recombinant Ganoderma lucidium Immunomodulatory Protein by Bacillus subtilis and Lactococcus lactis. Appl. Environ. Microbiol. 2008, 74(4), 1039–1049.
  • Harris, R. P.; Kilby, P. M. Amino Acid Misincorporation in Recombinant Biopharmaceutical Products. Curr. Opin. Biotechnol. 2014, 30, 45–50.
  • Marin, M. Folding at the Rhythm of the Rare Codon Beat. Biotechnol. J. 2008, 3(8), 1047–1057.
  • Menzella, H. G. Comparison of Two Codon Optimization Strategies to Enhance Recombinant Protein Production in Escherichia coli. Microb. Cell Factories. 2011, 10(1), 15.
  • Nakahama, K.; Miyazaki, T.; Kikuchi, M. A Promoter for Bacillus subtilis Expression Vector. Gene 1985, 36(1–2), 179–182. DOI: 10.1016/0378-1119(85)90083-6.
  • Rojas Contreras, J. A.; Pedraza-Reyes, M.; Ordoñez, L. G.; Estrada, N. U.; Barba de la Rosa, A. P.; De León-Rodríguez, A. Replicative and Integrative Plasmids for Production of Human Interferon Gamma in Bacillus subtilis. Plasmid [Internet]. 2010, 64(3), 170–176. Available from: http://www.sciencedirect.com/science/article/pii/S0147619×10000661.
  • Van Dijl, J. M.; Hecker, M. Bacillus subtilis: From Soil Bacterium to Super-Secreting Cell Factory. Microb. Cell Factories. 2013, 12(1), 3.
  • Gasser, B.; Saloheimo, M.; Rinas, U.; Dragosits, M.; Rodríguez-Carmona, E.; Baumann, K.; Giuliani, M.; Parrilli, E.; Branduardi, P.; Lang, C.; et al. Protein Folding and Conformational Stress in Microbial Cells Producing Recombinant Proteins: A Host Comparative Overview. Microb. Cell Factories. 2008, 7, 11.
  • Iafolla, M. A. J.; Mazumder, M.; Sardana, V.; Velauthapillai, T.; Pannu, K.; McMillen, D. R. Dark Proteins: Effect of Inclusion Body Formation on Quantification of Protein Expression. Proteins Struct. Funct. Bioinforma. 2008, 72(4), 1233–1242. DOI: 10.1002/prot.22024.
  • Jhamb, K.; Sahoo, D. K. Production of Soluble Recombinant Proteins in Escherichia coli: Effects of Process Conditions and Chaperone Co-Expression on Cell Growth and Production of Xylanase. Bioresour. Technol. 2012, 123, 135–143. DOI: 10.1016/j.biortech.2012.07.011.
  • Blommel, P. G.; Becker, K. J.; Duvnjak, P.; Fox, B. G. Enhanced Bacterial Protein Expression During Auto-Induction Obtained by Alteration of Lac Repressor Dosage and Medium Composition. Biotechnol. Prog. 2007, 23(3), 585–598.
  • González-García, R. A.; Garcia-Peña, E. I.; Salgado-Manjarrez, E.; Aranda-Barradas, J. S. Metabolic Flux Distribution and Thermodynamic Analysis of Green Fluorescent Protein Production in Recombinant Escherichia coli: The Effect of Carbon Source and CO2 Partial Pressure. Biotechnol. Bioprocess Eng. 2014, 18(6), 1049–1061. DOI: 10.1007/s12257-013-0277-5.
  • Shiloach, J.; Fass, R. Growing E. coli to High Cell Density—A Historical Perspective on Method Development. Biotechnol. Adv. 2005, 23(5), 345–357.
  • Wang, H.; Wang, F.; Wang, W.; Yao, X.; Wei, D.; Cheng, H.; Deng, Z. Improving the Expression of Recombinant Proteins in E. coli BL21 (DE3) under Acetate Stress: An Alkaline pH Shift Approach. PLoS ONE 2014, 9(11), e112777.
  • Çalık, P.; Özdamar, T. H. Carbon Sources Affect Metabolic Capacities of Bacillus Species for the Production of Industrial Enzymes: Theoretical Analyses for Serine and Neutral Proteases and α-Amylase. Biochem. Eng. J. 2001, 8(1), 61–81.
  • Çalik, P.; Özdamar, T. H. Metabolic Network Analysis for Human Therapeutic Protein Productions: Effects of the P/O Ratio. In Merten, O.-W., Mattanovich, D., Lang, C., Larsson, G., Neubauer, P., Porro, D., et al., Eds.; Springer: Netherlands, Berlin Heidelberg, 2001; pp 277–288.
  • Fürch, T.; Wittmann, C.; Wang, W.; Franco-Lara, E.; Jahn, D.; Deckwer, W.-D. Effect of Different Carbon Sources on Central Metabolic Fluxes and the Recombinant Production of a Hydrolase from Thermobifida fusca in Bacillus megaterium. J. Biotechnol. 2007, 132(4), 385–394.
  • Sauer, U.; Eikmanns, B. J. The PEP—Pyruvate—Oxaloacetate Node as the Switch Point for Carbon Flux Distribution in Bacteria: We Dedicate this Paper to Rudolf K. Thauer, Director of the Max-Planck-Institute for Terrestrial Microbiology in Marburg, Germany, on the Occasion of his 65th Birthday. FEMS Microbiol. Rev. 2005, 29(4), 765–794. DOI: 10.1016/j.femsre.2004.11.002.
  • Gonsky, R.; Deem, R. L.; Bream, J. H.; Lee, D. H.; Young, H. A.; Targan, S. R. Mucosa-Specific Targets for Regulation of IFN-Gamma Expression: Lamina Propria T Cells Use Different Cis-Elements than Peripheral Blood T Cells to Regulate Transactivation of IFN-Gamma Expression. J. Immunol. (Baltimore, Md.: 1950) 2000, 164(3), 1399–1407.
  • Nakamura, Y.; Gojobori, T.; Ikemura, T. Codon Usage Tabulated from International DNA Sequence Databases: Status for the Year 2000. Nucleic Acids Res. 2000, 28(1), 292–292.
  • Puigbò, P.; Bravo, I. G.; Garcia-Vallve, S. CAIcal: A Combined Set of Tools to Assess Codon Usage Adaptation. Biol Direct. 2008, 3(1), 38. DOI: 10.1186/1745-6150-3-38.
  • Sharp, P. M.; Li, W.-H. The Codon Adaptation Index-A Measure of Directional Synonymous Codon Usage Bias, and Its Potential Applications. Nucleic Acids Res. 1987, 15(3), 1281–1295.
  • Xia, X. An Improved Implementation of Codon Adaptation Index. Evol Bioinforma. 2007, 3, 53–58.
  • Mathews, D. H.; Sabina, J.; Zuker, M.; Turner, D. H. Expanded Sequence Dependence of Thermodynamic Parameters Improves Prediction of RNA Secondary Structure. J. Mol. Biol. 1999, 288(5), 911–940.
  • Wuchty, S.; Fontana, W.; Hofacker, I. L.; Schuster, P. Complete Suboptimal Folding of RNA and the Stability of Secondary Structures. Biopolymers 1999, 49(2), 145–165.
  • Struhl, K. Enzymatic Manipulation of DNA and RNA; John Wiley & Sons, Inc., New Jersey, 2001.
  • Vojcic, L.; Despotovic, D.; Martinez, R.; Maurer, K.-H.; Schwaneberg, U. An Efficient Transformation Method for Bacillus subtilis DB104. Appl. Microbiol. Biotechnol. 2012, 94(2), 487–493.
  • Moszer, I.; Rocha, E. P.; Danchin, A. Codon Usage and Lateral Gene Transfer in Bacillus subtilis. Curr. Opin. Microbiol. 1999, 2(5), 524–528.
  • Phan, T. T. P.; Nguyen, H. D.; Schumann, W. Novel Plasmid-Based Expression Vectors for Intra- and Extracellular Production of Recombinant Proteins in Bacillus subtilis. Protein Expr. Purif. 2006, 46(2), 189–195.
  • Boël, G.; Letso, R.; Neely, H.; Price, W. N.; Wong, K.-H.; Su, M.; Luff, J. D.; Valecha, M.; Everett, J. K.; Acton, T. B.; et al. Codon Influence on Protein Expression in E. coli Correlates with mRNA Levels. Nature 2016, 529(7586), 358–363.
  • Jia, M.; Li, Y. The Relationship among Gene Expression, Folding Free Energy and Codon Usage Bias in Escherichia coli. FEBS Lett. 2005, 579(24), 5333–5337.
  • Kim, M.-S.; Jang, J.-H.; Kim, Y.-W. Overproduction of a Thermostable 4-α-Glucanotransferase by Codon Optimization at N-Terminus Region. J. Sci. Food Agric. 2013, 93(11), 2683–2690.
  • Li, Z.; Nimtz, M.; Rinas, U. The Metabolic Potential of Escherichia coli BL21 in Defined and Rich Medium. Microb. Cell Factories. 2014, 13(1), 45.
  • Stephanopoulos, G. N.; Aristidou, A. A.; Nielsen, J. Chapter 1 - The Essence of Metabolic Engineering. In Nielsen, G. N. S. A. A., Eds.; Academic Press: San Diego, 1998. pp 1–20.
  • Tripathi, N. K.; Shrivastva, A.; Biswal, K. C.; Rao, P. L. Methods: Optimization of Culture Medium for Production of Recombinant Dengue Protein in Escherichia coli. Ind. Biotechnol. 2009, 5(3), 179–183. DOI: 10.1089/ind.2009.3.179.
  • Matsui, T.; Sato, H.; Sato, S.; Mukataka, S.; Takahashi, J. Effects of Nutritional Conditions on Plasmid Stability and Production of Tryptophan Synthase by a Recombinant Escherichia coli. Agric. Biol. Chem. 1990, 54(3), 619–624.
  • Klumpp, S.; Hwa, T. Bacterial Growth: Global Effects on Gene Expression, Growth Feedback and Proteome Partition. Curr. Opin. Biotechnol. 2014, 28C, 96–102.
  • Saier, Jr M. H.; Goldman, S. R.; Maile, R. R.; Moreno, M. S.; Weyler, W.; Yang, N.; Paulsen, I. T. Transport Capabilities Encoded within the Bacillus subtilis Genome. J. Mol. Microbiol. Biotechnol. 2002, 4(1), 37–67.
  • Wu, S.-C.; Yeung, J. C.; Duan, Y.; Ye, R.; Szarka, S. J.; Habibi, H. R.; Wong, S.-L. Functional Production and Characterization of a Fibrin-Specific Single-Chain Antibody Fragment from Bacillus subtilis: Effects of Molecular Chaperones and a Wall-Bound Protease on Antibody Fragment Production. Appl. Environ. Microbiol. 2002, 68(7), 3261–3269. Available from: http://aem.asm.org/content/68/7/3261
  • Lam, K. H. E.; Chow, K. C.; Wong, W. K. R. Construction of an Efficient Bacillus subtilis System for Extracellular Production of Heterologous Proteins. J. Biotechnol. 1998, 63(3), 167–177. Available from: http://www.sciencedirect.com/science/article/pii/S0168165698000418
  • Kwong, K. W. Y.; Ng, K. L.; Lam, C. C.; Wang, Y. Y.; Wong, W. K. R. Authentic Human Basic Fibroblast Growth Factor Produced by Secretion in Bacillus subtilis. Appl. Microbiol. Biotechnol. 2013, 97(15), 6803–6811. Available from: http://link.springer.com/article/10.1007/s00253–012-4592-0
  • Kakeshita, H.; Kageyama, Y.; Ara, K.; Ozaki, K.; Nakamura, K. Propeptide of Bacillus subtilis Amylase Enhances Extracellular Production of Human Interferon-α in Bacillus subtilis. Appl. Microbiol. Biotechnol. 2010, 89(5), 1509–1517. Available from: http://link.springer.com/article/10.1007/s00253–010-2954-z
  • Kakeshita, H.; Kageyama, Y.; Endo, K.; Tohata, M.; Ara, K.; Ozaki, K.; Nakamura, K. Secretion of Biologically-Active Human Interferon-β by Bacillus subtilis. Biotechnol. Lett. 2011, 33(9), 1847–1852. Available from: http://link.springer.com/article/10.1007/s10529–011-0636-2
  • Nguyen, H. D.; Phan, T. T. P.; Schumann, W. Analysis and Application of Bacillus subtilis Sortases to Anchor Recombinant Proteins on the Cell Wall. AMB Express 2011, 1(1), 1–11. Available from: http://link.springer.com/article/10.1186/2191–0855-1-22
  • Nguyen, H. D.; Phan, T. T. P.; Schumann, W. Expression Vectors for the Rapid Purification of Recombinant Proteins in Bacillus subtilis. Curr. Microbiol. 2007, 55(2), 89–93. Available from: http://link.springer.com/article/10.1007/s00284–006-0419-5
  • Gonsky, R.; Deem, R. L.; Bream, J. H.; Lee, D. H.; Young, H. A.; Targan, S. R. Mucosa-Specific Targets for Regulation of IFN-Gamma Expression: Lamina Propria T Cells Use Different Cis-Elements than Peripheral Blood T Cells to Regulate Transactivation of IFN-Gamma Expression. J. Immunol. (Baltimore, Md.: 1950) 2000, 164(3), 1399–1407.
  • Zhang, H.; Fu, G.; Zhang, D. Cloning, Characterization, and Production of a Novel Lysozyme by Different Expression Hosts. J. Microbiol. Biotechnol. 2014, 24, 1405–1412. DOI: 10.4014/jmb.1404.04039.
  • Song, Y.; Nikoloff, J. M.; Zhang, D. Improving Protein Production on the Level of Regulation of both Expression and Secretion Pathways in Bacillus subtilis. J. Microbiol. Biotechnol. 2015, 25, 963–977.
  • Gruber, A. R.; Lorenz, R.; Bernhart, S. H.; Neuböck, R.; Hofacker, I. L. The Vienna RNA Website. Nucleic Acids Res. 2008, 36, W70–W74.
  • Borkowski, O.; Goelzer, A.; Schaffer, M.; Calabre, M.; Mäder, U.; Aymerich, S.; Jules, M.; Fromion, V. Translation Elicits a Growth Rate‐Dependent, Genome‐Wide, Differential Protein Production in Bacillus subtilis. Mol. Syst. Biol. 2016, 12, 870. DOI: 10.15252/msb.20156608.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.