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PMID: 2467900 Published · ppublish English Journal Article

Secretory leukocyte protease inhibitor binding to mRNA and DNA as a possible cause of toxicity to Escherichia coli.

Journal of bacteriology ·Vol. 171 ·No. 4 ·1989-04-00 ·Pages 2166-72

Miller KW, Evans RJ, Eisenberg SP, Thompson RC

Abstract

The expression of the positively charged human protein secretory leukocyte protease inhibitor (SLPI) in Escherichia coli causes severe cellular toxicity. After induction of SLPI synthesis in a high-level-expression strain, SGE61, the growth of the strain is arrested and total protein and RNA synthesis rates decline by 60 to 70%. The mechanism of SLPI-mediated inhibition of macromolecular synthesis was examined in cell-free transcription-translation systems. SLPI proved to be a potent inhibitor of translation in vitro. When SLPI was added to translation reactions at SLPI/mRNA ratios attained during maximal SLPI accumulation in SGE61, translation of a test mRNA was inhibited by 75%. The mechanism of translation inhibition was deduced from in vitro experiments showing that SLPI bound to mRNA and interfered with the interaction of RNA-metabolizing enzymes, such as RNase. In addition, SLPI bound to DNA in vitro, but transcription was not inhibited as strongly in cell-free reactions as it was in SGE61. Similar nucleic acid-binding and translation inhibition properties were displayed in vitro by another basic protein, chicken egg white lysozyme, but were not displayed by the relatively acidic protein bovine serum albumin. On the basis of these results, we concluded that SLPI binds to nucleic acids via charge interactions and inhibits translation by competing with ribosomes for binding to mRNA. Since SLPI-mRNA and SLPI-DNA binding occurred at SLPI/mRNA and SLPI/DNA ratios existing in SGE61, nucleic acid binding may contribute to the toxicity of SLPI to E. coli. These results indicate that, in general, high-level expression of basic recombinant proteins in E. coli may be problematic.

MeSH Terms
Bacterial Proteins/biosynthesis Cell-Free System DNA, Bacterial/metabolism DNA-Binding Proteins/toxicity Escherichia coli/drug effects Muramidase/metabolism Protease Inhibitors/toxicity Protein Biosynthesis/drug effects Proteinase Inhibitory Proteins, Secretory Proteins/toxicity RNA, Bacterial/biosynthesis RNA, Messenger/metabolism Recombinant Proteins/toxicity Ribosomes/metabolism Secretory Leukocyte Peptidase Inhibitor Transcription, Genetic/drug effects
Chemicals
Bacterial Proteins DNA, Bacterial DNA-Binding Proteins Protease Inhibitors Proteinase Inhibitory Proteins, Secretory Proteins RNA, Bacterial RNA, Messenger Recombinant Proteins SLPI protein, human Secretory Leukocyte Peptidase Inhibitor Muramidase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Miller K W
Human Pharmaceuticals Section, Synergen, Inc., Boulder, Colorado 80301.
Evans R J
Eisenberg S P
Thompson R C
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Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1989-04-00
Pages
2166-72
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC209873
Subset
IM
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