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Volume 272, Number 28, Issue of July 11, 1997 pp. 17502-17510
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.

The RNA Molecule CsrB Binds to the Global Regulatory Protein CsrA and Antagonizes Its Activity in Escherichia coli

(Received for publication, January 27, 1997, and in revised form, April 3, 1997)

Mu Ya Liu , Gaojun Gui , Bangdong Wei , James F. Preston III^¶ , Lawrence Oakford , Ümit Yüksel ^** , David P. Giedroc and Tony Romeo ^**

From the Departments of  Microbiology and Immunology,  Anatomy and Cell Biology, and ^** Biochemistry and Molecular Biology, University of North Texas Health Science Center at Fort Worth, Fort Worth, Texas 76107-2699, the ^¶ Department of Microbiology and Cell Science, University of Florida, Gainesville, Florida 32611-0100, and the  Department of Biochemistry and Biophysics, Texas A & M University, College Station, Texas 77843-2128

The RNA-binding protein CsrA (carbon storage regulator) is a new kind of global regulator, which facilitates specific mRNA decay. A recombinant CsrA protein containing a metal-binding affinity tag (CsrA-H6) was purified to homogeneity and authenticated by N-terminal sequencing, matrix-assisted laser desorption/ionization time of flight mass spectrometry, and other studies. This protein was entirely contained within a globular complex of approximately 18 CsrA-H6 subunits and a single ~350-nucleotide RNA, CsrB. cDNA cloning and nucleotide sequencing revealed that the csrB gene is located downstream from syd in the 64-min region of the Escherichia coli K-12 genome and contains no open reading frames. The purified CsrA-CsrB ribonucleoprotein complex was active in regulating glg (glycogen biosynthesis) gene expression in vitro, as was the RNA-free form of the CsrA protein. Overexpression of csrB enhanced glycogen accumulation in E. coli, a stationary phase process that is repressed by CsrA. Thus, CsrB RNA is a second component of the Csr system, which binds to CsrA and antagonizes its effects on gene expression. A model for regulatory interactions in Csr is presented, which also explains previous observations on the homologous system in Erwinia carotovora. A highly repeated nucleotide sequence located within predicted stem-loops and other single-stranded regions of CsrB, CAGGA(U/A/C)G, is a plausible CsrA-binding element.

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