FinO/ProQ-family proteins: an evolutionary perspective

Smirnov, Alexandre; Liao, Zhen

doi:10.1042/bsr20220313

Cited by 7 publications

(9 citation statements)

References 110 publications

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“…The incomplete complementary pairing of most ncRNAs with the target mRNA sequence can lead to two results: (1) Blocking the ribosome binding sites and suppressing translation; (2) Secondary structure melting, exposing the nucleose binding site and translation start site, leading to translation activation ( Vogel and Sharma, 2005 ; Fröhlich and Vogel, 2009 ). Moreover, since the instabilized base pairing between the ncRNAs and their target mRNAs, the RNA chaperone protein Hfq, binding protein Fino/ProQ family, CsrA/RsmA family and other regulators usually facilitate imperfect base pairing between ncRNAs and mRNAs, leading to regulate the translation initiation frequency or the stability of target mRNAs ( Liao and Smirnov, 2023 ; Wang et al., 2023 ; Yu and Zhao, 2023 ). In this chapter, we will explore some research on ncRNAs that regulate the mechanisms of AMR from two perspectives.…”

Section: Bacterial Epigenetics Mediating Antibiotic Resistancementioning

confidence: 99%

Antimicrobial resistance and mechanisms of epigenetic regulation

Wang

2023

Front. Cell. Infect. Microbiol.

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The rampant use of antibiotics in animal husbandry, farming and clinical disease treatment has led to a significant issue with pathogen resistance worldwide over the past decades. The classical mechanisms of resistance typically investigate antimicrobial resistance resulting from natural resistance, mutation, gene transfer and other processes. However, the emergence and development of bacterial resistance cannot be fully explained from a genetic and biochemical standpoint. Evolution necessitates phenotypic variation, selection, and inheritance. There are indications that epigenetic modifications also play a role in antimicrobial resistance. This review will specifically focus on the effects of DNA modification, histone modification, rRNA methylation and the regulation of non-coding RNAs expression on antimicrobial resistance. In particular, we highlight critical work that how DNA methyltransferases and non-coding RNAs act as transcriptional regulators that allow bacteria to rapidly adapt to environmental changes and control their gene expressions to resist antibiotic stress. Additionally, it will delve into how Nucleolar-associated proteins in bacteria perform histone functions akin to eukaryotes. Epigenetics, a non-classical regulatory mechanism of bacterial resistance, may offer new avenues for antibiotic target selection and the development of novel antibiotics.

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Section: Bacterial Epigenetics Mediating Antibiotic Resistancementioning

confidence: 99%

Antimicrobial resistance and mechanisms of epigenetic regulation

Wang

2023

Front. Cell. Infect. Microbiol.

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“…The global RBP ProQ belongs to the ProQ/FinO protein family, members of which are found in many proteobacterial species ( 21 , 22 ). Global profiling in Salmonella and Escherichia coli ( E. coli ) has attributed hundreds of RNAs as ProQ ligands ( 23 – 26 ), the majority of which are sRNAs and mRNA 3′UTRs.…”

Section: Introductionmentioning

confidence: 99%

ProQ-dependent activation of Salmonella virulence genes mediated by post-transcriptional control of PhoP synthesis

Bergman,

Andresen,

Kjellin

et al. 2024

mSphere

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Gastrointestinal disease caused by Salmonella enterica is associated with the pathogen’s ability to replicate within epithelial cells and macrophages. Upon host cell entry, the bacteria express a type-three secretion system encoded within Salmonella pathogenicity island 2, through which host-manipulating effector proteins are secreted to establish a stable intracellular niche. Transcription of this intracellular virulence program is activated by the PhoPQ two-component system that senses the low pH and the reduced magnesium concentration of host cell vacuoles. In addition to transcriptional control, Salmonella commonly employ RNA-binding proteins (RBPs) and small regulatory RNAs (sRNAs) to regulate gene expression at the post-transcriptional level. ProQ is a globally acting RBP in Salmonella that promotes expression of the intracellular virulence program, but its RNA repertoire has previously been characterized only under standard laboratory growth conditions. Here, we provide a high-resolution ProQ interactome during conditions mimicking the environment of the Salmonella -containing vacuole (SCV), revealing hundreds of previously unknown ProQ binding sites in sRNAs and mRNA 3′UTRs. ProQ positively affected both the levels and the stability of many sRNA ligands, some of which were previously shown to associate with the well-studied and infection-relevant RBP Hfq. We further show that ProQ activates the expression of PhoP at the post-transcriptional level, which, in turn, leads to upregulation of the intracellular virulence program. IMPORTANCE Salmonella enterica is a major pathogen responsible for foodborne gastroenteritis, and a leading model organism for genetic and molecular studies of bacterial virulence mechanisms. One key trait of this pathogen is the ability to survive within infected host cells. During infection, the bacteria employ a type three secretion system that deliver effector proteins to target and manipulate host cell processes. The transcriptional regulation of this virulence program is well understood. By contrast, the factors and mechanisms operating at the post-transcriptional level to control virulence gene expression are less clear. In this study, we have charted the global RNA ligand repertoire of the RNA-binding protein ProQ during in vitro conditions mimicking the host cell environment. This identified hundreds of binding sites and revealed ProQ-dependent stabilization of intracellular-specific small RNAs. Importantly, we show that ProQ post-transcriptionally activates the expression of PhoP, a master transcriptional activator of intracellular virulence in Salmonella .

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“…Typically, the activity of trans-encoded sRNAs in Gram-negative bacteria depends on RNA-binding proteins (RBPs) (Vogel and Luisi, 2011; Holmqvist and Vogel, 2018; Felden and Augagneur, 2021; Olejniczak et al ., 2022; Liao and Smirnov, 2023; Papenfort and Melamed, 2023). For example, in Enterobacteriaceae the protein Hfq is frequently required for mediating sRNA-mRNA annealing (Vogel and Luisi, 2011; Santiago-Frangos and Woodson, 2018).…”

Section: Introductionmentioning

confidence: 99%

Global analysis of the RNA-RNA interactome inAcinetobacter baumanniiAB5075 uncovers a small regulatory RNA repressing the virulence-related outer membrane protein CarO

Hamrock,

Ryan,

Shaibah

et al. 2023

Preprint

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Acinetobacter baumanniiis an opportunistic Gram-negative pathogen that infects critically ill patients. The emergence of antimicrobial resistantA. baumanniihas exacerbated the need to functionally characterise environmental adaptation, antibiotic resistance and pathogenicity of this organism and their genetic regulators to inform intervention strategies. Critical to rapid adaptation to changing environments in bacteria are small regulatory RNAs (sRNAs), however, the role that sRNAs play in the biology ofA. baumanniiis poorly understood. To assess the regulatory function of sRNAs and to uncover their RNA interaction partners inA. baumannii, we employed an RNA proximity ligation and sequencing method (Hi-GRIL-seq) in three different environmental conditions. We found that 40 sRNA candidates were ligated to sRNA-RNA chimeric sequencing reads, suggesting that sRNA-mediated gene regulation is pervasive inA. baumanniiand that sRNAs act as direct regulators of mRNA molecules through antisense base-pairing. In-depth characterisation uncovered the sRNA Aar to be a post-transcriptional regulator of four mRNA targets including that of the outer membrane protein CarO and the siderophore receptor BfnH. We show that Aar initiates base-pairing with these mRNA molecules using a conserved seed region of nine nucleotides, sequestering the ribosome binding sites and inhibiting translation. Aar is differentially expressed in response to multiple stress stimuli suggesting a role in fine-tuning translation of the Aar-target molecules inA. baumanniiunder hostile conditions. Together, our study provides mechanistic insights into sRNA-mediated gene expression control inA. baumanniiand represents a valuable resource for future RNA-centric research endeavours in this ESKAPE pathogen.

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FinO/ProQ-family proteins: an evolutionary perspective

Cited by 7 publications

References 110 publications

Antimicrobial resistance and mechanisms of epigenetic regulation

Antimicrobial resistance and mechanisms of epigenetic regulation

ProQ-dependent activation of Salmonella virulence genes mediated by post-transcriptional control of PhoP synthesis

Global analysis of the RNA-RNA interactome inAcinetobacter baumanniiAB5075 uncovers a small regulatory RNA repressing the virulence-related outer membrane protein CarO

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