Riboregulation of Enolase 1 activity controls glycolysis and embryonic stem cell differentiation

Huppertz, Ina; Perez-Perri, Joel I.; Mantas, Panagiotis; Sekaran, Thileepan; Schwarzl, Thomas; Russo, Francesco; Ferring-Appel, Dunja; Koskova, Zuzana; Dimitrova-Paternoga, Lyudmila; Kafkia, Eleni; Hennig, Janosch; Neveu, Pierre; Patil, Kiran R.; Hentze, Matthias W.

doi:10.1016/j.molcel.2022.05.019

Cited by 70 publications

(34 citation statements)

References 73 publications

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“…Alternatively, the RNAs may riboregulate the enzymes that they bind to. Riboregulation has recently been shown for human enolase 1 (Huppertz et al2022), and the human small non-coding vtRNA1-1 has been identified to regulate mammalian autophagy by binding to the receptor protein p62 (Horos et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Small non-coding RNA Interactome Capture reveals pervasive, carbon source-dependent tRNA engagement of yeast glycolytic enzymes

Asencio

Schwarzl

Sahadevan

et al. 2022

Preprint

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Small non-coding RNAs fulfill key functions in cellular and organismal biology, typically working in concert with RNA-binding proteins (RBPs). While proteome-wide methodologies have enormously expanded the repertoire of known RBPs, these methods do not distinguish RBPs binding to small non-coding RNAs from the rest. To specifically identify this relevant subclass of RBPs, we developed small non-coding RNA interactome capture (snRIC2C) based on the differential RNA-binding capacity of silica matrices (2C). We define the S. cerevisiae proteome of nearly 300 proteins that specifically binds to RNAs smaller than 200 nucleotides in length (snRBPs), identifying informative distinctions from the total RNA-binding proteome determined in parallel. Strikingly, the snRBPs include most glycolytic enzymes from yeast. With further methodological developments using silica matrices, 12 tRNAs were identified as specific binders of the glycolytic enzyme GAPDH. We show that tRNA engagement of GAPDH is carbon source-dependent and regulated by the RNA polymerase III repressor Maf1, suggesting a regulatory interaction between glycolysis and RNA polymerase III activity. We conclude that snRIC2C and other 2C-derived methods greatly facilitate the study of RBPs, revealing previously unrecognised interactions.

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Section: Discussionmentioning

confidence: 99%

Small non-coding RNA Interactome Capture reveals pervasive, carbon source-dependent tRNA engagement of yeast glycolytic enzymes

Asencio

Schwarzl

Sahadevan

et al. 2022

Preprint

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“…ENO1 from Rattus norvegicus acts as CUG triplet repeat-binding protein in gel shift assays (Hernández-Pérez et al, 2011). Moreover, using eCLIP, Huppertz et al described about 2000 RNA binding sites of human ENO1 predominantly in the 5'-UTR of target transcripts in HeLa cells (Huppertz et al, 2022). They could show, that human ENO1 is target of complex riboregulation.…”

Section: Enolasementioning

confidence: 99%

“…More direct regulation of metabolic activity in situ might occur through competitive inhibition when RNA binding site is identical to the substrate or co-factor binding site as in case of human ENO1 (Huppertz et al, 2022) or through allosteric inhibition as observed for prokaryotic pyruvate kinase (Yu et al, 2021). Dynamic binding of metabolic enzymes to RNA would regulate the availability of active enzyme.…”

Section: Different Sites For Moonlighting Of Glycolytic Enzymes In Th...mentioning

confidence: 99%

“…Also malonylation was shown to regulate RNA binding activity of mammalian GAPDH (Galván-Peña et al, 2019). Riboregulation of human ENO1 is controlled by acetylation (Huppertz et al, 2022). This modification presents an additional link to metabolite concentrations as acetylation of proteins is based on sufficient supply with acetyl-CoA (Xing and Poirier, 2012).…”

Section: How To Coordinate Rna Binding Activity Of Glycolytic Enzymesmentioning

confidence: 99%

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The mutual interaction of glycolytic enzymes and RNA in post-transcriptional regulation

Wegener

Dietz

2022

RNA

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About three decades ago, researchers suggested that metabolic enzymes participate in cellular processes that are unrelated to their catalytic activity, and the term moonlighting functions was proposed. Recently developed advanced technologies in the field of RNA interactome capture now unveil the unexpected RNA binding activity of many metabolic enzymes, as exemplified here for the enzymes of glycolysis. Although for most of these proteins precise binding mechanism, binding conditions and physiological relevance of the binding events still awaits in depth clarification, several well-explored examples demonstrate that metabolic enzymes hold crucial functions in post-transcriptional regulation of protein synthesis. This widely conserved RNA-binding function of glycolytic enzymes plays major roles in controlling cell activities. Best-explored examples are glyceraldehyde 3-phsohphate dehydrogenase, enolase, phosphoglycerate kinase and pyruvate kinase. This review summarizes the current knowledge about the RNA-binding activity of the ten core enzymes of glycolysis in plant, yeast and animal cells, its regulation and physiological relevance. Apparently, a tight bidirectional regulation connects core metabolism and RNA biology forcing us to rethink long-established functional singularities.

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“…KAT7 is a major member of the MYST family of histone acetyltransferases and plays an important role in DNA replication, gene transcription, and embryonic development [ 52 , 53 , 54 ]. ENO1 can regulate the process related to glycolysis as a key enzyme in the glycolytic pathway [ 55 ]. Therefore, targeting ENO1 might improve the sensitivity to chemotherapy and reduce the resistance to oxaliplatin and 5-fluorouracil (5-FU) by inhibiting F. nucleatum -induced glycolysis in CRC patients [ 49 ].…”

Section: Microbial Regulation Of Crc Mediated By Lncrnasmentioning

confidence: 99%

Effects of Long Non-Coding RNAs Induced by the Gut Microbiome on Regulating the Development of Colorectal Cancer

Fan

Xing

Jiang

et al. 2022

Cancers

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Although an imbalanced gut microbiome is closely associated with colorectal cancer (CRC), how the gut microbiome affects CRC is not known. Long non-coding RNAs (lncRNAs) can affect important cellular functions such as cell division, proliferation, and apoptosis. The abnormal expression of lncRNAs can promote CRC cell growth, proliferation, and metastasis, mediating the effects of the gut microbiome on CRC. Generally, the gut microbiome regulates the lncRNAs expression, which subsequently impacts the host transcriptome to change the expression of downstream target molecules, ultimately resulting in the development and progression of CRC. We focused on the important role of the microbiome in CRC and their effects on CRC-related lncRNAs. We also reviewed the impact of the two main pathogenic bacteria, Fusobacterium nucleatum and enterotoxigenic Bacteroides fragilis, and metabolites of the gut microbiome, butyrate, and lipopolysaccharide, on lncRNAs. Finally, available therapies that target the gut microbiome and lncRNAs to prevent and treat CRC were proposed.

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Riboregulation of Enolase 1 activity controls glycolysis and embryonic stem cell differentiation

Cited by 70 publications

References 73 publications

Small non-coding RNA Interactome Capture reveals pervasive, carbon source-dependent tRNA engagement of yeast glycolytic enzymes

Small non-coding RNA Interactome Capture reveals pervasive, carbon source-dependent tRNA engagement of yeast glycolytic enzymes

The mutual interaction of glycolytic enzymes and RNA in post-transcriptional regulation

Effects of Long Non-Coding RNAs Induced by the Gut Microbiome on Regulating the Development of Colorectal Cancer

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