A 3′ UTR-Derived Small RNA Provides the Regulatory Noncoding Arm of the Inner Membrane Stress Response

Chao, Yapeng; Vogel, Jörg

doi:10.1016/j.molcel.2015.12.023

Cited by 163 publications

(212 citation statements)

References 71 publications

(86 reference statements)

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“…These results suggest that the Cpx response monitors the biogenesis of membrane-bound protein complexes like NDH-I and cytochrome bo 3 through a signal that is specific to IM proteins. In this regard, it is of interest that Chao and Vogel have shown that the small RNA (sRNA) CpxQ, encoded in the 3= end of the cpxP mRNA, serves to downregulate the expression of several integral IM proteins (50). Additionally, Grabowicz et al recently showed that downregulation of the periplasmic chaperone Skp by the CpxQ sRNA is likely needed to stem the aberrant insertion of OMPs into the cytoplasmic membrane (58).…”

Section: Discussionmentioning

confidence: 99%

A Bacterial Stress Response Regulates Respiratory Protein Complexes To Control Envelope Stress Adaptation

et al. 2017

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The Cpx envelope stress response mediates adaptation to stresses that affect protein folding within the envelope of Gram-negative bacteria. Recent transcriptome analyses revealed that the Cpx response impacts genes that affect multiple cellular functions predominantly associated with the cytoplasmic membrane. In this study, we examined the connection between the Cpx response and the respiratory complexes NADH dehydrogenase I and cytochrome bo 3 in enteropathogenic Escherichia coli. We found that the Cpx response directly represses the transcription of the nuo and cyo operons and that Cpx-mediated repression of these complexes confers adaptation to stresses that compromise envelope integrity. Furthermore, we found that the activity of the aerobic electron transport chain is reduced in E. coli lacking a functional Cpx response despite no change in the transcription of either the nuo or the cyo operon. Finally, we show that expression of NADH dehydrogenase I and cytochrome bo 3 contributes to basal Cpx pathway activity and that overproduction of individual subunits can influence pathway activation. Our results demonstrate that the Cpx response gauges and adjusts the expression, and possibly the function, of inner membrane protein complexes to enable adaptation to envelope stress.IMPORTANCE Bacterial stress responses allow microbes to survive environmental transitions and conditions, such as those encountered during infection and colonization, that would otherwise kill them. Enteric microbes that inhabit or infect the gut are exposed to a plethora of stresses, including changes in pH, nutrient composition, and the presence of other bacteria and toxic compounds. Bacteria detect and adapt to many of these conditions by using envelope stress responses that measure the presence of stressors in the outermost compartment of the bacterium by monitoring its physiology. The Cpx envelope stress response plays a role in antibiotic resistance and host colonization, and we have shown that it regulates many functions at the bacterial inner membrane. In this report, we describe a novel role for the Cpx response in sensing and controlling the expression of large, multiprotein respiratory complexes at the cytoplasmic membrane of Escherichia coli. The significance of our research is that it will increase our understanding of how these stress responses are involved in antibiotic resistance and the mechanisms used by bacteria to colonize the gut.KEYWORDS envelope stress response, NADH dehydrogenase I, cytochrome bo 3 , membrane protein biogenesis, Cpx envelope stress response, NADH dehydrogenase, cytochrome oxidase, inner membrane, protein complex, protein folding, protein localization, respiration, two-component regulatory systems G ram-negative bacteria are characterized by the structure of their cell envelope, which consists of the inner membrane (IM), the outer membrane, and the peptidoglycan layer within the periplasmic space. Of these, the IM contains the greatest protein diversity (1). Proteins that reside within the IM...

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Section: Discussionmentioning

confidence: 99%

A Bacterial Stress Response Regulates Respiratory Protein Complexes To Control Envelope Stress Adaptation

et al. 2017

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“…It is tempting to speculate that these RNAs produced in axons and dendrites could signal back to inform the cell bodies on the metabolic status of the peripheral compartments. An interesting example of how 3′UTR fragments functionally cooperate with the protein encoded by the parental mRNA has been provided by Vogel and co-workers (Chao and Vogel, 2016). They showed that in Salmonella enterica , RNAse E cleaves the 3′UTR of the CpxP mRNA, a gene that encodes a protein activated during inner membrane stress.…”

Section: Cytoplasmic Cleavage Of 3′utrsmentioning

confidence: 99%

Post-transcriptional Processing of mRNA in Neurons: The Vestiges of the RNA World Drive Transcriptome Diversity

Andreassi

Crerar

Riccio

2018

Front. Mol. Neurosci.

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Neurons are morphologically complex cells that rely on the compartmentalization of protein expression to develop and maintain their extraordinary cytoarchitecture. This formidable task is achieved, at least in part, by targeting mRNA to subcellular compartments where they are rapidly translated. mRNA transcripts are the conveyor of genetic information from DNA to the translational machinery, however, they are also endowed with additional functions linked to both the coding sequence (open reading frame, or ORF) and the flanking 5′ and 3′ untranslated regions (UTRs), that may harbor coding-independent functions. In this review, we will highlight recent evidences supporting new coding-dependent and -independent functions of mRNA and discuss how nuclear and cytoplasmic post-transcriptional modifications of mRNA contribute to localization and translation in mammalian cells with specific emphasis on neurons. We also describe recently developed techniques that can be employed to study RNA dynamics at subcellular level in eukaryotic cells in developing and regenerating neurons.

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“…The work presented in this issue by Raivio and coworkers (5), combined with recent work on the roles of the CpxQ sRNA (14,15), suggests that for Cpx as well, downregulation of the clients of the Cpx-induced proteins defines critical components that the regulatory response protects. As with the sigma E response, the induced arm of the Cpx response includes chaperones and protein foldases to promote correct protein folding or to help degrade proteins that are beyond chaperone-induced repair (16).…”

mentioning

confidence: 97%

“…Most notable is CpxQ, an Hfq-binding sRNA encoded at the 3= end of the cpxP gene, one of the most highly induced promoters of the Cpx response (14,15). Overexpression of CpxQ downregulated multiple mRNAs in Salmonella; the mRNAs were enriched for those encoding proteins with IM or periplasmic localization.…”

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confidence: 99%

Stress Reduction, Bacterial Style

Gottesman

2017

J Bacteriol

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Bacteria have robust responses to a variety of stresses. In particular, bacteria like Escherichia coli have multiple cell envelope stress responses, and generally we evaluate what these responses are doing by the repair systems they induce. However, probably at least as important in interpreting what is being sensed as stress are the genes that these stress systems downregulate, directly or indirectly. This is discussed here for the Cpx and sigma E systems of E. coli.

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A 3′ UTR-Derived Small RNA Provides the Regulatory Noncoding Arm of the Inner Membrane Stress Response

Cited by 163 publications

References 71 publications

A Bacterial Stress Response Regulates Respiratory Protein Complexes To Control Envelope Stress Adaptation

A Bacterial Stress Response Regulates Respiratory Protein Complexes To Control Envelope Stress Adaptation

Post-transcriptional Processing of mRNA in Neurons: The Vestiges of the RNA World Drive Transcriptome Diversity

Stress Reduction, Bacterial Style

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