1887

Abstract

Proteasomes are self-compartmentalizing proteases first discovered in eukaryotes but also occurring in archaea and in bacteria belonging to the order . In bacteria, proteasomes have so far no known function. In order to evaluate the influence of the 20S proteasome on the production of heterologous proteins by TK24, the production of a number of heterologous proteins, including soluble human tumour necrosis factor receptor II (shuTNFRII) and salmon calcitonin (sCT), was compared with the wild-type TK24, a proteasome-deficient mutant designated PRO41 and a strain complemented for the disrupted proteasome genes (strain PRO41R). cells lacking intact proteasome genes are phenotypically indistinguishable from the wild-type or the complemented strain containing functional proteasomes. Using the expression and secretion signals of the subtilisin inhibitor of CBS762.70 (Vsi) for shuTNFRII and those of tyrosinase of (MelC1) for the production of sCT, both proteins were secreted in significantly higher amounts in the strain PRO41 than in the wild-type TK24 or the complemented strain PRO41R. However, the secretion of other heterologous proteins such as shuTNFRI was not enhanced in the proteasome-deficient strain. This suggests that TK24 can degrade some heterologous proteins in a proteasome-dependent fashion. The proteasome-deficient strain may therefore be useful for the efficient production of these heterologous proteins.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28034-0
2005-09-01
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/9/mic1513137.html?itemId=/content/journal/micro/10.1099/mic.0.28034-0&mimeType=html&fmt=ahah

References

  1. Bernan, V., Filpula, D., Herber, W., Bibb, M. & Katz, E. ( 1985; ). The nucleotide sequence of the tyrosinase gene from Streptomyces antibioticus and characterization of the gene product. Gene 37, 101–110.[CrossRef]
    [Google Scholar]
  2. Binnie, C., Butler, M. J., Aphale, J. S., Bourgault, R., DiZonno, M. A., Krygsman, P., Liao, L., Walczyk, E. & Malek, L. T. ( 1995; ). Isolation and characterization of two genes encoding proteases associated with the mycelium of Streptomyces lividans 66. J Bacteriol 177, 6033–6040.
    [Google Scholar]
  3. Binnie, C., Cossar, J. D. & Stewart, D. I. H. ( 1997; ). Heterologous biopharmaceutical protein expression in Streptomyces. Trends Biotechnol 15, 315–320.[CrossRef]
    [Google Scholar]
  4. Bolhuis, A., Matzen, A., Hyyrylainen, H. L. & 7 other authors ( 1999a; ). Signal peptide peptidase- and ClpP-like proteins of Bacillus subtilis required for efficient translocation and processing of secretory proteins. J Biol Chem 274, 24585–24592.[CrossRef]
    [Google Scholar]
  5. Bolhuis, A., Tjalsma, H., Smith, H. E., de Jong, A., Meima, R., Venema, G., Bron, S. & van Dijl, J. M. ( 1999b; ). Evaluation of bottlenecks in the late stages of protein secretion in Bacillus subtilis. Appl Environ Microbiol 65, 2934–2941.
    [Google Scholar]
  6. Butler, M. J., Aphale, J. S., Binnie, C., DiZonno, M. A., Krygsman, P., Soltes, G. A., Walczyk, E. & Malek, L. T. ( 1994; ). The aminopeptidase N-encoding pepN gene of Streptomyces lividans 66. Gene 141, 115–119.[CrossRef]
    [Google Scholar]
  7. Butler, M. J., Binnie, C., DiZonno, M. A., Krygsman, P., Soltes, G. A., Soostmeyer, G., Walczyk, E. & Malek, L. T. ( 1995; ). Cloning and characterization of a gene encoding a secreted tripeptidyl aminopeptidase from Streptomyces lividans 66. Appl Environ Microbiol 61, 3145–3150.
    [Google Scholar]
  8. Chang, S.-Y. & Chang, S. ( 1988; ). Secretion of heterologous proteins in Streptomyces lividans. In Biology of Actinomycetes '88, pp. 103–107. Edited by Y. Okami, T. Beppu & H. Ogawara. Tokyo, Japan: Japan Scientific Society Press.
  9. Dahlmann, B., Kopp, F., Kuehn, L., Niedel, B., Pfeifer, G., Hegerl, R. & Baumeister, W. ( 1989; ). The multicatalytic proteinase (prosome) is ubiquitous from eukaryotes to archaebacteria. FEBS Lett 251, 125–131.[CrossRef]
    [Google Scholar]
  10. Darwin, K. H., Ehrt, S., Gutierrez-Ramos, J. C., Weich, N. & Nathan, C. F. ( 2003; ). The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302, 1963–1966.[CrossRef]
    [Google Scholar]
  11. De Mot, R., Nagy, I., Walz, J. & Baumeister, W. ( 1999; ). Proteasomes and other self-compartmentalizing proteases in prokaryotes. Trends Microbiol 7, 88–92.[CrossRef]
    [Google Scholar]
  12. Denis, F. & Brzezinski, R. ( 1992; ). A versatile shuttle cosmid vector for use in Escherichia coli and actinomycetes. Gene 111, 115–118.[CrossRef]
    [Google Scholar]
  13. Engler-Blum, G., Meier, M., Frank, J. & Muller, G. A. ( 1993; ). Reduction of background problems in nonradioactive Northern and Southern blot analyses enables higher sensitivity than 32P-based hybridizations. Anal Biochem 210, 235–244.[CrossRef]
    [Google Scholar]
  14. Fornwald, J. A., Donovan, M. J., Gerber, R., Keller, J., Taylor, D. P., Arcuri, E. J. & Brawner, M. E. ( 1993; ). Soluble forms of the human T cell receptor CD4 are efficiently expressed by Streptomyces lividans. Bio/Technology 11, 1031–1036.[CrossRef]
    [Google Scholar]
  15. Gill, R. T., Valdes, J. J. & Bentley, W. E. ( 2000; ). A comparative study of global stress gene regulation in response to overexpression of recombinant proteins in Escherichia coli. Metab Eng 2, 178–189.[CrossRef]
    [Google Scholar]
  16. Hochstrasser, M. ( 1995; ). Ubiquitin, proteasomes and the regulation of intracellular protein degradation. Curr Opin Cell Biol 7, 215–223.[CrossRef]
    [Google Scholar]
  17. Hoeltke, H.-J., Schneider, S., Ettl, I., Binsack, R., Obermaier, I., Seller, M. & Sagner, G. ( 1995; ). Rapid, highly sensitive detection of digoxigenin-labeled nucleic acids by improved chemiluminescent alkaline phosphatase substrates. Biochemica 1, 17–20.
    [Google Scholar]
  18. Hong, B., Wu, B. & Li, Y. ( 2003; ). Production of C-terminal amidated recombinant salmon calcitonin in Streptomyces lividans. Appl Biochem Biotechnol 110, 113–123.[CrossRef]
    [Google Scholar]
  19. Kawamoto, S. & Ochi, K. ( 1998; ). Comparative ribosomal protein (L11 and L30) sequence analyses of several Streptomyces spp. commonly used in genetic studies. Int J Syst Bacteriol 48, 597–600.[CrossRef]
    [Google Scholar]
  20. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F. & Hopwood, D. A. ( 2000; ). Practical Streptomyces Genetics. Norwich, UK: John Innes Foundation.
  21. Knipfer, N. & Shrader, T. E. ( 1997; ). Inactivation of the 20S proteasome in Mycobacterium smegmatis. Mol Microbiol 25, 375–383.[CrossRef]
    [Google Scholar]
  22. Korn, F., Weingartner, B. & Kutzner, H. J. ( 1978; ). A study of twenty actinophages: morphology, serological relationship and host range. In Genetics of the Actinomycetales, pp. 251–270. Edited by E. Freechsen, I. Tarnak. & J. H. Thumin. New York: Gustav Fisher Verlag.
  23. Krieger, T. J., Bartfeld, D., Jenish, D. L. & Hadary, D. ( 1994; ). Purification and characterization of a novel tripeptidyl aminopeptidase from Streptomyces lividans 66. FEBS Lett 352, 385–388.[CrossRef]
    [Google Scholar]
  24. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  25. Lammertyn, E. ( 2000; ). Isolation and characterization of a novel subtilisin inhibitor from Streptomyces venezuelae and evaluation of its regulatory sequences for heterologous protein secretion by Streptomyces lividans. PhD thesis, Katholieke Universiteit Leuven, Leuven, Belgium.
  26. Lammertyn, E., Van Mellaert, L., Schacht, S., Dillen, C., Sablon, E., Van Broekhoven, A. & Anné, J. ( 1997; ). Evaluation of a novel subtilisin inhibitor gene and mutant derivatives for the expression and secretion of mouse tumor necrosis factor alpha by Streptomyces lividans. Appl Environ Microbiol 63, 1808–1813.
    [Google Scholar]
  27. Lichenstein, H. S., Busse, L. A., Smith, G. A., Narhi, L. O., McGinley, M. O., Rohde, M. F., Katzowitz, J. L. & Zukowski, M. M. ( 1992; ). Cloning and characterization of a gene encoding extracellular metalloprotease from Streptomyces lividans. Gene 111, 125–130.[CrossRef]
    [Google Scholar]
  28. Mori, H. & Ito, K. ( 2001; ). The Sec protein-translocation pathway. Trends Microbiol 9, 494–500.[CrossRef]
    [Google Scholar]
  29. Nagy, I., Tamura, T., Vanderleyden, J., Baumeister, W. & De Mot, R. ( 1998; ). The 20S proteasome of Streptomyces celicolor. J Bacteriol 180, 5448–5453.
    [Google Scholar]
  30. Nagy, I., Banerjee, T., Tamura, T., Schoofs, G., Gils, A., Proost, P., Tamura, N., Baumeister, W. & De Mot, R. ( 2003; ). Characterization of a novel intracellular endopeptidase of the α/β hydrolase family from Streptomyces coelicolor A3(2). J Bacteriol 185, 496–503.[CrossRef]
    [Google Scholar]
  31. Pouch, M.-N., Cournoyer, B. & Baumeister, W. ( 2000; ). Characterization of the 20S proteasome from the actinomycetes Frankia. Mol Microbiol 35, 368–377.[CrossRef]
    [Google Scholar]
  32. Pozidis, C., Lammertyn, E., Politou, A. S., Anné, J., Tsiftsoglou, A. S., Sianidis, G. & Economou, A. ( 2001; ). Protein secretion biotechnology using Streptomyces lividans: large-scale production of functional trimeric tumor necrosis factor alpha. Biotechnol Bioeng 72, 611–619.[CrossRef]
    [Google Scholar]
  33. Richardson, M. A., Kuhstoss, S., Solenberg, P., Schaus, N. A. & Rao, R. N. ( 1987; ). A new shuttle cosmid vector, pKC505, for streptomycetes: its use in the cloning of three different spiramycin-resistance genes from a Streptomyces ambofaciens library. Gene 61, 231–241.[CrossRef]
    [Google Scholar]
  34. Ruepp, A., Eckerskorn, C., Bogyo, M. & Baumeister, W. ( 1998; ). Proteasome function is dispensable under normal but not under heat shock conditions in Thermoplasma acidophilum. FEBS Lett 425, 87–90.[CrossRef]
    [Google Scholar]
  35. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  36. Sassetti, C. M., Boyd, D. H. & Rubin, E. J. ( 2003; ). Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48, 77–84.[CrossRef]
    [Google Scholar]
  37. Schaerlaekens, K., Schierova, M., Lammertyn, E., Geukens, N., Anné, J. & Van Mellaert, L. ( 2001; ). Twin-arginine translocation pathway in Streptomyces lividans. J Bacteriol 183, 6727–6732.[CrossRef]
    [Google Scholar]
  38. Schaerlaekens, K., Lammertyn, E., Geukens, N., De Keersmaeker, S., Anné, J. & Van Mellaert, L. ( 2004; ). Comparison of the Sec and Tat secretion pathways for heterologous protein production by Streptomyces lividans. J Biotechnol 112, 279–288.[CrossRef]
    [Google Scholar]
  39. Tamura, T., Nagy, I., Lupas, A., Lottspeich, F., Cejka, Z., Schoofs, G., Tanaka, K., De Mot, R. & Baumeister, W. ( 1995; ). The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr Biol 5, 766–774.[CrossRef]
    [Google Scholar]
  40. Van Mellaert, L. & Anné, J. ( 2001; ). Gram-positive bacteria for the heterologous production of biopharmaceutical compounds. In Novel Frontiers in the Production of Compounds for Biomedical Use, vol. 1, pp. 277–300. Edited by A. Van Broekhoven, F. Shapiro & J. Anné. Kluwer Academic.
  41. Van Mellaert, L., Dillen, C., Proost, P. & 7 other authors ( 1994; ). Efficient secretion of biologically active mouse tumor necrosis factor by Streptomyces lividans. Gene 150, 153–158.[CrossRef]
    [Google Scholar]
  42. Van Mellaert, L., Lammertyn, E., Schacht, S. & 8 other authors ( 1998; ). Molecular characterization of a novel subtilisin inhibitor protein produced by Streptomyces venezuelae CBS762.70. DNA Sequence 9, 19–30.
    [Google Scholar]
  43. Voges, D., Zwickl, P. & Baumeister, W. ( 1999; ). The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem 68, 1015–1068.[CrossRef]
    [Google Scholar]
  44. Ward, J. M., Janssen, G. R., Kieser, T., Bibb, M. J., Buttner, M. J. & Bibb, M. J. ( 1986; ). Construction and characterisation of a series of multi-copy promoter-probe plasmid vectors for Streptomyces using the aminoglycoside phosphotransferase gene from Tn5 as indicator. Mol Gen Genet 203, 468–478.[CrossRef]
    [Google Scholar]
  45. Wu, X.-C., Lee, W., Tran, L. & Wong, S.-L. ( 1991; ). Engineering a Bacillus subtilis expression-secretion system with a strain deficient in six extracellular proteases. J Bacteriol 173, 4952–4958.
    [Google Scholar]
  46. Zuhl, F., Seemuller, E., Golbik, R. & Baumeister, W. ( 1997; ). Dissecting the assembly pathway of the 20S proteasome. FEBS Lett 418, 189–194.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28034-0
Loading
/content/journal/micro/10.1099/mic.0.28034-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error