Global RNA Fold and Molecular Recognition for a pfl Riboswitch Bound to ZMP, a Master Regulator of One-Carbon Metabolism

Ren, Aiming; Rajashankar, Kanagalaghatta R.; Patel, Dinshaw J.

doi:10.1016/j.str.2015.05.016

Title: Global RNA Fold and Molecular Recognition for a pfl Riboswitch Bound to ZMP, a Master Regulator of One-Carbon Metabolism

Abstract

ZTP, the pyrophosphorylated analog of ZMP (5- amino-4-imidazole carboxamide ribose-5'-monophosphate), was identified as an alarmone that senses 10-formyl-tetrahydroflate deficiency in bacteria. Recently, a pfl riboswitch was identified that selectively binds ZMP and regulates genes associated with purine biosynthesis and one-carbon metabolism. Here we report on the structure of the ZMP-bound Thermosinus carboxydivorans pfl riboswitch sensing domain, thereby defining the pseudoknot-based tertiary RNA fold, the binding-pocket architecture, and principles underlying ligand recognition specificity. Molecular recognition involves shape complementarity, with the ZMP 5-amino and carboxamide groups paired with the Watson-Crick edge of an invariant uracil, and the imidazole ring sandwiched between guanines, while the sugar hydroxyls form intermolecular hydrogen bond contacts. The burial of the ZMP base and ribose moieties, together with unanticipated coordination of the carboxamide by Mg²⁺, contrasts with exposure of the 5'-phosphate to solvent. Lastly, our studies highlight the principles underlying RNA-based recognition of ZMP, a master regulator of one-carbon metabolism.

Authors:: Ren, Aiming; Rajashankar, Kanagalaghatta R.; Patel, Dinshaw J.

Publication Date:: Sat Aug 01 00:00:00 EDT 2015

Research Org.:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Org.:: USDOE Office of Science (SC); National Institutes of Health (NIH)

OSTI Identifier:: 1433725

Alternate Identifier(s):: OSTI ID: 1209696

Grant/Contract Number:: AC02-06CH11357; S10 RR029205; P41 GM103403

Resource Type:: Published Article

Journal Name:: Structure

Additional Journal Information:: Journal Name: Structure Journal Volume: 23 Journal Issue: 8; Journal ID: ISSN 0969-2126

Publisher:: Elsevier

Country of Publication:: United Kingdom

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

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                    Ren, Aiming, Rajashankar, Kanagalaghatta R., and Patel, Dinshaw J. Global RNA Fold and Molecular Recognition for a pfl Riboswitch Bound to ZMP, a Master Regulator of One-Carbon Metabolism.  United Kingdom: N. p., 2015. 
Web.  doi:10.1016/j.str.2015.05.016.

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                    Ren, Aiming, Rajashankar, Kanagalaghatta R., & Patel, Dinshaw J. Global RNA Fold and Molecular Recognition for a pfl Riboswitch Bound to ZMP, a Master Regulator of One-Carbon Metabolism.  United Kingdom.  https://doi.org/10.1016/j.str.2015.05.016

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                    Ren, Aiming, Rajashankar, Kanagalaghatta R., and Patel, Dinshaw J. Sat .  
"Global RNA Fold and Molecular Recognition for a pfl Riboswitch Bound to ZMP, a Master Regulator of One-Carbon Metabolism".  United Kingdom.  https://doi.org/10.1016/j.str.2015.05.016.

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@article{osti_1433725,

  title        = {Global RNA Fold and Molecular Recognition for a pfl Riboswitch Bound to ZMP, a Master Regulator of One-Carbon Metabolism},

  author       = {Ren, Aiming and Rajashankar, Kanagalaghatta R. and Patel, Dinshaw J.},

  abstractNote = {ZTP, the pyrophosphorylated analog of ZMP (5- amino-4-imidazole carboxamide ribose-5'-monophosphate), was identified as an alarmone that senses 10-formyl-tetrahydroflate deficiency in bacteria. Recently, a pfl riboswitch was identified that selectively binds ZMP and regulates genes associated with purine biosynthesis and one-carbon metabolism. Here we report on the structure of the ZMP-bound Thermosinus carboxydivorans pfl riboswitch sensing domain, thereby defining the pseudoknot-based tertiary RNA fold, the binding-pocket architecture, and principles underlying ligand recognition specificity. Molecular recognition involves shape complementarity, with the ZMP 5-amino and carboxamide groups paired with the Watson-Crick edge of an invariant uracil, and the imidazole ring sandwiched between guanines, while the sugar hydroxyls form intermolecular hydrogen bond contacts. The burial of the ZMP base and ribose moieties, together with unanticipated coordination of the carboxamide by Mg2+, contrasts with exposure of the 5'-phosphate to solvent. Lastly, our studies highlight the principles underlying RNA-based recognition of ZMP, a master regulator of one-carbon metabolism.},

  doi          = {10.1016/j.str.2015.05.016},

  journal      = {Structure},

  number       = 8,

  volume       = 23,

  place        = {United Kingdom},

  year         = {Sat Aug 01 00:00:00 EDT 2015},

  month        = {Sat Aug 01 00:00:00 EDT 2015}

}

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Works referencing / citing this record:

A ligand-gated strand displacement mechanism for ZTP riboswitch transcription control
journal, October 2019

Strobel, Eric J.; Cheng, Luyi; Berman, Katherine E.
Nature Chemical Biology, Vol. 15, Issue 11
DOI: 10.1038/s41589-019-0382-7

The ancient alarmone ZTP and zinc homeostasis in Bacillus subtilis
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Nies, Dietrich H.
Molecular Microbiology, Vol. 112, Issue 3
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Specific features of l-histidine production by Escherichia coli concerned with feedback control of AICAR formation and inorganic phosphate/metal transport
journal, March 2018

Malykh, Evgeniya A.; Butov, Ivan A.; Ravcheeva, Anna B.
Microbial Cell Factories, Vol. 17, Issue 1
DOI: 10.1186/s12934-018-0890-2

Riboswitch diversity and distribution
journal, April 2017

McCown, Phillip J.; Corbino, Keith A.; Stav, Shira
RNA, Vol. 23, Issue 7
DOI: 10.1261/rna.061234.117

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Similar Records

Title: Global RNA Fold and Molecular Recognition for a pfl Riboswitch Bound to ZMP, a Master Regulator of One-Carbon Metabolism

Abstract

Citation Formats

A ligand-gated strand displacement mechanism for ZTP riboswitch transcription control journal, October 2019

The ancient alarmone ZTP and zinc homeostasis in Bacillus subtilis journal, July 2019

Specific features of l-histidine production by Escherichia coli concerned with feedback control of AICAR formation and inorganic phosphate/metal transport journal, March 2018

Riboswitch diversity and distribution journal, April 2017

A ligand-gated strand displacement mechanism for ZTP riboswitch transcription control
journal, October 2019

The ancient alarmone ZTP and zinc homeostasis in Bacillus subtilis
journal, July 2019

Specific features of l-histidine production by Escherichia coli concerned with feedback control of AICAR formation and inorganic phosphate/metal transport
journal, March 2018

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journal, April 2017