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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