Reversible acetylation on Lys501 regulates the activity of RNase II

RNase II, a 3′ to 5′ processive exoribonuclease, is the major hydrolytic enzyme in Escherichia coli accounting for ∼90% of the total activity. Despite its importance, little is actually known about regulation of this enzyme. We show here that one residue, Lys501, is acetylated in RNase II. This modification, reversibly controlled by the acetyltransferase Pka, and the deacetylase CobB, affects binding of the substrate and thus decreases the catalytic activity of RNase II. As a consequence, the steady-state level of target RNAs of RNase II may be altered in the cells. We also find that under conditions of slowed growth, the acetylation level of RNase II is elevated and the activity of RNase II decreases, emphasizing the importance of this regulatory process. These findings indicate that acetylation can regulate the activity of a bacterial ribonuclease.

[1]  Dylan J. Sorensen,et al.  Protein acetylation dynamics in response to carbon overflow in Escherichia coli , 2015, Molecular microbiology.

[2]  C. Condon,et al.  sRNA and mRNA turnover in Gram-positive bacteria. , 2015, FEMS microbiology reviews.

[3]  M. Deutscher.  How bacterial cells keep ribonucleases under control. , 2015, FEMS microbiology reviews.

[4]  M. Deutscher.  Twenty years of bacterial RNases and RNA processing: how we've matured , 2015, RNA.

[5]  J. Belasco,et al.  Messenger RNA degradation in bacterial cells. , 2014, Annual review of genetics.

[6]  A. Taghbalout,et al.  The Escherichia coli major exoribonuclease RNase II is a component of the RNA degradosome , 2014, Bioscience reports.

[7]  Bao Wang,et al.  Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores , 2013, PLoS genetics.

[8]  Hening Lin,et al.  Identification of Lysine Succinylation Substrates and the Succinylation Regulatory Enzyme CobB in Escherichia coli* , 2013, Molecular & Cellular Proteomics.

[9]  M. Deutscher,et al.  Ribosomes Regulate the Stability and Action of the Exoribonuclease RNase R* , 2013, The Journal of Biological Chemistry.

[10]  H. Putzer,et al.  Initiation of mRNA decay in bacteria , 2013, Cellular and Molecular Life Sciences.

[11]  Chunaram Choudhary,et al.  Acetyl-phosphate is a critical determinant of lysine acetylation in E. coli. , 2013, Molecular cell.

[12]  B. Luisi,et al.  Licensing and due process in the turnover of bacterial RNA , 2013, RNA biology.

[13]  Yue Chen,et al.  Comprehensive profiling of protein lysine acetylation in Escherichia coli. , 2013, Journal of proteome research.

[14]  M. Deutscher,et al.  Post-translational modification of RNase R is regulated by stress-dependent reduction in the acetylating enzyme Pka (YfiQ). , 2012, RNA.

[15]  M. Deutscher,et al.  Acetylation regulates the stability of a bacterial protein: growth stage-dependent modification of RNase R. , 2011, Molecular cell.

[16]  M. Deutscher,et al.  Degradation of ribosomal RNA during starvation: comparison to quality control during steady-state growth and a role for RNase PH. , 2011, RNA.

[17]  Kun-Liang Guan,et al.  Regulation of intermediary metabolism by protein acetylation. , 2011, Trends in biochemical sciences.

[18]  M. Deutscher,et al.  A Novel Mechanism for Ribonuclease Regulation , 2010, The Journal of Biological Chemistry.

[19]  A. Wolfe,et al.  Bacterial protein acetylation: the dawning of a new age , 2010, Molecular microbiology.

[20]  M. Dines,et al.  Acetylation represses the binding of CheY to its target proteins , 2010, Molecular microbiology.

[21]  L. Bi,et al.  CobB regulates Escherichia coli chemotaxis by deacetylating the response regulator CheY , 2010, Molecular microbiology.

[22]  M. Deutscher,et al.  RNase R is a highly unstable protein regulated by growth phase and stress. , 2010, RNA.

[23]  Guo-Ping Zhao,et al.  Acetylation of Metabolic Enzymes Coordinates Carbon Source Utilization and Metabolic Flux , 2010, Science.

[24]  J. Escalante‐Semerena.  N ε-Lysine Acetylation Control Conserved in All Three Life Domains: The relative simplicity of studying microbes could prove critical for understanding this posttranslational modification system. , 2010, Microbe.

[25]  M. Deutscher,et al.  The Roles of Individual Domains of RNase R in Substrate Binding and Exoribonuclease Activity , 2009, Journal of Biological Chemistry.

[26]  M. Deutscher,et al.  Structural basis for processivity and single-strand specificity of RNase II. , 2006, Molecular cell.

[27]  M. A. Carrondo,et al.  Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex , 2006, Nature.

[28]  H. Mori,et al.  Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection , 2006, Molecular systems biology.

[29]  M. Deutscher,et al.  Elevation of RNase R in Response to Multiple Stress Conditions* , 2005, Journal of Biological Chemistry.

[30]  L. Guarente,et al.  The Sir2 family of protein deacetylases. , 2004, Annual review of biochemistry.

[31]  Xiang-Jiao Yang.  The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. , 2004, Nucleic acids research.

[32]  S. R. Kushner,et al.  Genomic analysis in Escherichia coli demonstrates differential roles for polynucleotide phosphorylase and RNase II in mRNA abundance and decay , 2003, Molecular microbiology.

[33]  M. Deutscher,et al.  Purification and Characterization of the Escherichia coli Exoribonuclease RNase R , 2002, The Journal of Biological Chemistry.

[34]  C. Arraiano,et al.  RNase II levels change according to the growth conditions: characterization of gmr, a new Escherichia coli gene involved in the modulation of RNase II , 2001, Molecular microbiology.

[35]  C. Arraiano,et al.  RNase II removes the oligo(A) tails that destabilize the rpsO mRNA of Escherichia coli. , 2000, RNA.

[36]  B. Wanner,et al.  One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  D. Kennell,et al.  The reaction mechanism of ribonuclease II and its interaction with nucleic acid secondary structures. , 1999, Biochimica et biophysica acta.

[38]  K. Rudd,et al.  The vacB Gene Required for Virulence inShigella flexneri and Escherichia coli Encodes the Exoribonuclease RNase R* , 1998, The Journal of Biological Chemistry.

[39]  C. Arraiano,et al.  PNPase modulates RNase II expression in Escherichia coli: implications for mRNA decay and cell metabolism , 1996, Molecular microbiology.

[40]  J. Plumbridge,et al.  Escherichia coli RNase II: characterization of the promoters involved in the transcription of rnb. , 1996, Microbiology.

[41]  C. Arraiano,et al.  The role of endonucleases in the expression of ribonuclease II in Escherichia coli. , 1995, FEMS microbiology letters.

[42]  M. Deutscher,et al.  Enzymatic basis for hydrolytic versus phosphorolytic mRNA degradation in Escherichia coli and Bacillus subtilis. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[43]  R. Kaplan,et al.  Accumulation of nucleotides by starved Escherichia coli cells as a probe for the involvement of ribonucleases in ribonucleic acid degradation , 1977, Journal of bacteriology.

[44]  M. Singer,et al.  The processive degradation of individual polyribonucleotide chains. I. Escherichia coli ribonuclease II. , 1968, The Journal of biological chemistry.