Substrate-dependent Effects of Quaternary Structure on RNase E Activity

Overview

Journal Genes Dev

Specialty Molecular Biology

Date 2021 Jan 15

PMID 33446571

Citations 4

Authors

Christopher J Moore

Hayoung Go

Eunkyoung Shin

Hye-Jeong Ha

Saemee Song

Nam-Chul Ha

Yong-Hak Kim

Stanley N Cohen

Kangseok Lee

Affiliations

Soon will be listed here.

Abstract

RNase E is an essential, multifunctional ribonuclease encoded in by the gene. Structural analysis indicates that the ribonucleolytic activity of this enzyme is conferred by -encoded polypeptide chains that (1) dimerize to form a catalytic site at the protein-protein interface, and (2) multimerize further to generate a tetrameric quaternary structure consisting of two dimerized Rne-peptide chains. We identify here a mutation in the Rne protein's catalytic region (E429G), as well as a bacterial cell wall peptidoglycan hydrolase (Amidase C [AmiC]), that selectively affect the specific activity of the RNase E enzyme on long RNA substrates, but not on short synthetic oligonucleotides, by enhancing enzyme multimerization. Unlike the increase in specific activity that accompanies concentration-induced multimerization, enhanced multimerization associated with either the E429G mutation or interaction of the Rne protein with AmiC is independent of the substrate's 5' terminus phosphorylation state. Our findings reveal a previously unsuspected substrate length-dependent regulatory role for RNase E quaternary structure and identify -acting and -acting factors that mediate such regulation.

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References

McDowall K, Kaberdin V, Wu S, Cohen S, Lin-Chao S . Site-specific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature. 1995; 374(6519):287-90. DOI: 10.1038/374287a0. View

Ray B, Singh B, Roy M, Apirion D . Ribonuclease E is involved in the processing of 5-S rRNA from a number of rRNA transcription units. Eur J Biochem. 1982; 125(2):283-9. DOI: 10.1111/j.1432-1033.1982.tb06680.x. View

Singh D, Chang S, Lin P, Averina O, Kaberdin V, Lin-Chao S . Regulation of ribonuclease E activity by the L4 ribosomal protein of Escherichia coli. Proc Natl Acad Sci U S A. 2009; 106(3):864-9. PMC: 2626609. DOI: 10.1073/pnas.0810205106. View

Caruthers J, Feng Y, McKay D, Cohen S . Retention of core catalytic functions by a conserved minimal ribonuclease E peptide that lacks the domain required for tetramer formation. J Biol Chem. 2006; 281(37):27046-51. DOI: 10.1074/jbc.M602467200. View

Liou G, Jane W, Cohen S, Lin N, Lin-Chao S . RNA degradosomes exist in vivo in Escherichia coli as multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E. Proc Natl Acad Sci U S A. 2001; 98(1):63-8. PMC: 14545. DOI: 10.1073/pnas.98.1.63. View

Garrey S, Blech M, Riffell J, Hankins J, Stickney L, Diver M . Substrate binding and active site residues in RNases E and G: role of the 5'-sensor. J Biol Chem. 2009; 284(46):31843-50. PMC: 2797255. DOI: 10.1074/jbc.M109.063263. View

Kim S, Kim H, Park I, Lee Y . Mutational analysis of RNA structures and sequences postulated to affect 3' processing of M1 RNA, the RNA component of Escherichia coli RNase P. J Biol Chem. 1996; 271(32):19330-7. DOI: 10.1074/jbc.271.32.19330. View

McWilliam H, Li W, Uludag M, Squizzato S, Park Y, Buso N . Analysis Tool Web Services from the EMBL-EBI. Nucleic Acids Res. 2013; 41(Web Server issue):W597-600. PMC: 3692137. DOI: 10.1093/nar/gkt376. View

Altschul S, Gish W, Miller W, Myers E, Lipman D . Basic local alignment search tool. J Mol Biol. 1990; 215(3):403-10. DOI: 10.1016/S0022-2836(05)80360-2. View

10.

Baek Y, Jang K, Lee H, Yoon S, Baek A, Lee K . The bacterial endoribonuclease RNase E can cleave RNA in the absence of the RNA chaperone Hfq. J Biol Chem. 2019; 294(44):16465-16478. PMC: 6827277. DOI: 10.1074/jbc.RA119.010105. View

11.

Sousa S, Marchand I, Dreyfus M . Autoregulation allows Escherichia coli RNase E to adjust continuously its synthesis to that of its substrates. Mol Microbiol. 2001; 42(3):867-78. DOI: 10.1046/j.1365-2958.2001.02687.x. View

12.

Koslover D, Callaghan A, Marcaida M, Garman E, Martick M, Scott W . The crystal structure of the Escherichia coli RNase E apoprotein and a mechanism for RNA degradation. Structure. 2008; 16(8):1238-44. PMC: 2631609. DOI: 10.1016/j.str.2008.04.017. View

13.

Callaghan A, Marcaida M, Stead J, McDowall K, Scott W, Luisi B . Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature. 2005; 437(7062):1187-91. DOI: 10.1038/nature04084. View

14.

Gao J, Lee K, Zhao M, Qiu J, Zhan X, Saxena A . Differential modulation of E. coli mRNA abundance by inhibitory proteins that alter the composition of the degradosome. Mol Microbiol. 2006; 61(2):394-406. DOI: 10.1111/j.1365-2958.2006.05246.x. View

15.

Jain C, Deana A, Belasco J . Consequences of RNase E scarcity in Escherichia coli. Mol Microbiol. 2002; 43(4):1053-64. DOI: 10.1046/j.1365-2958.2002.02808.x. View

16.

Ize B, Stanley N, Buchanan G, Palmer T . Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol Microbiol. 2003; 48(5):1183-93. DOI: 10.1046/j.1365-2958.2003.03504.x. View

17.

McDowall K, Cohen S . The N-terminal domain of the rne gene product has RNase E activity and is non-overlapping with the arginine-rich RNA-binding site. J Mol Biol. 1996; 255(3):349-55. DOI: 10.1006/jmbi.1996.0027. View

18.

Remy I, Michnick S . A highly sensitive protein-protein interaction assay based on Gaussia luciferase. Nat Methods. 2006; 3(12):977-9. DOI: 10.1038/nmeth979. View

19.

Jourdan S, Kime L, McDowall K . The sequence of sites recognised by a member of the RNase E/G family can control the maximal rate of cleavage, while a 5'-monophosphorylated end appears to function cooperatively in mediating RNA binding. Biochem Biophys Res Commun. 2009; 391(1):879-83. DOI: 10.1016/j.bbrc.2009.11.156. View

20.

Gopel Y, Papenfort K, Reichenbach B, Vogel J, Gorke B . Targeted decay of a regulatory small RNA by an adaptor protein for RNase E and counteraction by an anti-adaptor RNA. Genes Dev. 2013; 27(5):552-64. PMC: 3605468. DOI: 10.1101/gad.210112.112. View