DOI: 10.1073/pnas.98.1.63. RNA degradosomes exist<i>in vivo</i>in<i>Escherichia coli</i>as multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E

RNA degradosomes existin vivoinEscherichia colias multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E

10.1073/pnas.98.1.63

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

RNase E isolated fromEscherichia coliis contained in a multicomponent “degradosome” complex with other proteins implicated in RNA decay. Earlier work has shown that the C-terminal region of RNase E is a scaffold for the binding of degradosome components and has identified specific RNase E segments necessary for its interaction with polynucleotide phosphorylase (PNPase), RhlB RNA helicase, and enolase. Here, we report electron microscopy studies that use immunogold labeling and freeze–fracture methods to show that degradosomes existin vivoinE. colias multicomponent structures that associate with the cytoplasmic membrane via the N-terminal region of RNase E. Whereas PNPase and enolase are present inE. coliin large excess relative to RNase E and therefore are detected in cells largely as molecules unlinked to the RNase E scaffold, immunogold labeling and biochemical analyses show that helicase is present in approximately equimolar amounts to RNase E at all cell growth stages. Our findings, which establish the existence and cellular location of RNase E-based degradosomesin vivoinE. coli, also suggest that RNA processing and decay may occur at specific sites within cells.

Bibliography

Liou, G.-G., Jane, W.-N., Cohen, S. N., Lin, N.-S., & Lin-Chao, S. (2000). RNA degradosomes existin vivoinEscherichia colias multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E. Proceedings of the National Academy of Sciences, 98(1), 63â68.

Authors 5

Gunn-Guang Liou (first)
Wann-Neng Jane (additional)
Stanley N. Cohen (additional)
Na-Sheng Lin (additional)
Sue Lin-Chao (additional)

References 39 Referenced 119

10.1046/j.1365-2958.1997.5901947.x
10.1016/0092-8674(94)90363-8
10.1073/pnas.93.9.3865
10.1111/j.1365-2958.1994.tb01309.x
10.1038/381169a0
10.1101/gad.12.17.2770
10.1101/gad.13.19.2594
10.1016/S0092-8674(00)80922-8
10.1016/S0092-8674(00)80923-X
10.1016/S0092-8674(00)80929-0
10.1146/annurev.biochem.66.1.679
10.1073/pnas.95.6.3157
10.1128/jb.178.13.3917-3925.1996
10.1046/j.1365-2958.1999.01465.x
10.1073/pnas.95.20.11637
10.1074/jbc.271.22.13103
10.1006/jmbi.1996.0027
10.1038/374287a0
10.1074/jbc.270.44.26391
10.1073/pnas.82.4.1074
E Harlow, D Lane Antibodies: a laboratory manual (Cold Spring Harbor Lab. Press, Plainview, NY), pp. 53–137 (1988). / Antibodies: a laboratory manual by Harlow E (1988)
J J Bozzola, L D Russell Electron Microscopy Principles and Techniques for Biologists (Jones and Bartlett Publishers, London, 1999). / Electron Microscopy Principles and Techniques for Biologists by Bozzola J J (1999)
A D Hyatt Electron Microscopy in Biology, ed J R Harris (Oxford Univ. Press, New York), pp. 59–81 (1991). (10.1093/oso/9780199632190.003.0004) / Electron Microscopy in Biology by Hyatt A D (1991)
10.1177/41.10.8245409
N-S Lin, G-G Liou, C-C Chen, B-Y Chang Zool Stud 34, 142–143 (1995). / Zool Stud by Lin N-S (1995)
10.1016/S0022-5320(83)90082-5
10.1242/jcs.108.11.3443
10.1007/s004180050092
10.1093/infdis/173.3.684
10.1111/j.1574-6968.1999.tb13734.x
10.1128/jb.171.12.6600-6609.1989
10.1074/jbc.270.19.11078
10.1111/j.1365-2958.1991.tb01929.x
10.1093/emboj/18.10.2878
10.1128/jb.175.13.4245-4249.1993
M R Tock, A P W Walsh, G Carroll, K J McDowall J Bacteriol 275, 8726–8732 (2000). / J Bacteriol by Tock M R (2000)
10.1016/0378-1119(91)90578-Y
10.1007/s004380050352
10.1006/bbrc.1999.0806

Dates

Type	When
Created	13 years ago (July 30, 2012, 1:19 p.m.)
Deposited	1 year, 4 months ago (April 27, 2024, 7:18 p.m.)
Indexed	3 months ago (May 26, 2025, 12:07 p.m.)
Issued	24 years, 8 months ago (Dec. 26, 2000)
Published	24 years, 8 months ago (Dec. 26, 2000)
Published Online	24 years, 8 months ago (Dec. 26, 2000)
Published Print	24 years, 7 months ago (Jan. 2, 2001)

Funders 0

None

BibTeX

@article{Liou_2000, title={RNA degradosomes existin vivoinEscherichia colias multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E}, volume={98}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.98.1.63}, DOI={10.1073/pnas.98.1.63}, number={1}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Liou, Gunn-Guang and Jane, Wann-Neng and Cohen, Stanley N. and Lin, Na-Sheng and Lin-Chao, Sue}, year={2000}, month=dec, pages={63–68} }

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